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WYATT – 9780521130196 Cover C M Y K
WYATT Pheromones and Animal Behavior
Second edition
Pheromones and other
kinds of chemical
communication underlie
the behavior of all animals.
Building on the strengths
of the first edition, widely
recognized as the leading
text in the subject, this is a
comprehensive overview of
how pheromones work.
Extensively revised and
expanded to cover advances made over the last ten years, the book offers
a thorough exploration of the evolutionary and behavioral contexts
of chemical communication, along with a detailed introduction to the
molecular and neural basis of chemosensory perception. Its breadth of
coverage and readability make the book an unrivaled resource for students
and researchers in a range of fields from chemistry, genetics, genomics,
molecular biology, and neuroscience to ecology, evolution, and behavior.
“Wyatt takes us through a well-judged range of examples of some
amazing chemical communication strategies, from ants right up to
the scent of human attraction. The book is far-reaching, inspiring,
and brilliantly illustrated.”
Patrizia d’Ettorre, University of Paris 13, Sorbonne Paris Cité
“As Wyatt observes, we live in a chemical world, and this lucidly written
and intelligently illustrated book sets the nostrils aquiver as we catch
the scent of a new reality.”
David W. Macdonald, Wildlife Conservation Research Unit,
University of Oxford
“I cannot help thinking that I will cite this book in all research papers
that I will publish in the future.”
Kazushige Touhara, The University of Tokyo
“This thoroughly modern revision of the classic first edition is an
amazing journey through the landscape of pheromones… The book
is a must-read for any undergraduate or graduate student or working
scientist interested in a singular comprehensive resource on this
fascinating topic.”
Leslie B. Vosshall, HHMI-The Rockefeller University
TR ISTR AM D. WYATT is a
researcher at Oxford University’s
Department of Zoology, and an
Emeritus Fellow of Kellogg
College, Oxford.
Cover illustration
(front): ring-tailed lemur (Lemur
catta), smelling a small bush for
traces of scent from other lemurs,
Madagascar. © Anup Shah/The
Image Bank/Getty Images;
(back): the male silkmoth (Bombyx
mori) has elaborate antennae
covered with sensillae highly
sensitive to the female sex
pheromone, bombykol.
© Walter Leal.
Pheromones and
Animal Behavior
Chemical Signals and Signatures
TRISTRAM D. WYATT
Second edition
Cover designed by Hart McLeod Ltd
This sample from the book
contains the front matter,
Chapter 1, Index, and full
references.
You may share this freely
with colleagues and
students. (these and the
Appendix introducing
pheromone chemistry for
non-chemists are also
available free from
www.cambridge.org/
pheromones ). The book can
be ordered there or from
Amazon.com etc.
Pheromones and Animal Behavior
Chemical Signals and Signatures
SECOND EDITION
Pheromones and other kinds of chemical communication underlie the behavior of all animals.
Building on the strengths of the first edition, widely recognized as the leading text in the
subject, this is a comprehensive overview of how pheromones work.
Extensively revised and expanded to cover advances made over the last ten years, the book
offers a thorough exploration of the evolutionary and behavioral contexts of chemical
communication, along with a detailed introduction to the molecular and neural basis of
chemosensory perception. At a time of ever increasing specialization, Wyatt offers a unique
synthesis, integrating examples across the animal kingdom. A final chapter critically considers
human pheromones and the importance of olfaction to human biology. Its breadth of coverage
and readability make the book an unrivaled resource for students and researchers in a range of
fields from chemistry, genetics, genomics, molecular biology, and neuroscience to ecology,
evolution, and behavior.
A full list of the references from this book is available for download from www.cambridge.
org/pheromones.
Tristram D. Wyatt is a researcher at Oxford University’s Department of Zoology, and an Emeritus
Fellow of Kellogg College, Oxford. He is interested in how pheromones evolve throughout the
animal kingdom, at both molecular and behavioral levels. These broad interests give him a
unique vantage point, enabling him to draw together developments across the subject.
This sample from the book contains the front matter, Chapter 1, Index, and full references.
You may share this freely with colleagues and students. (these and the Appendix introducing
pheromone chemistry for non-chemists are also available free from
www.cambridge.org/pheromones ). The book can be ordered there or from Amazon.com etc.
Pheromones and
Animal Behavior
Chemical Signals and Signatures
SECOND EDITION
TRISTRAM D. WYATT
Department of Zoology and Kellogg College,
University of Oxford
University Printing House, Cambridge CB2 8BS, United Kingdom
Published in the United States of America by Cambridge University Press, New York
Cambridge University Press is part of the University of Cambridge.
It furthers the University’s mission by disseminating knowledge in the pursuit of
education, learning, and research at the highest international levels of excellence.
www.cambridge.org
Information on this title: www.cambridge.org/pheromones
©T.D. Wyatt 2014
First edition ©Cambridge University Press 2003
This publication is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without the written
permission of Cambridge University Press.
First published 2003
Second edition 2014
Printed in the United Kingdom by TJ International Ltd. Padstow Cornwall
A catalog record for this publication is available from the British Library
ISBN 978-0-521-11290-1 Hardback
ISBN 978-0-521-13019-6 Paperback
Additional resources for this publication at www.cambridge.org/pheromones
Cambridge University Press has no responsibility for the persistence or accuracy of
URLs for external or third-party internet websites referred to in this publication,
and does not guarantee that any content on such websites is, or will remain,
accurate or appropriate.
To Robert
CONTENTS
Preface page xi
Acknowledgments xv
List of SI prefixes xvi
List of abbreviations xvii
1 Animals in a chemical world 1
1.1 Intra-specific semiochemicals: pheromones
and signature mixtures 2
1.2 “Innateness”of pheromones 16
1.3 How pheromone signals evolve from chemical
cues 18
1.4 Pheromone diversity, specificity, and
speciation 24
1.5 Production of pheromones 31
1.6 Pheromones: signal honesty and costs 32
1.7 Chemical profiles from which signature
mixtures are learned for individual and colony
recognition 37
1.8 Differences in response to pheromones 43
1.9 Releaser and primer effects of
pheromones 43
1.10 Multimodal signals 44
1.11 Allohormone pheromones bypassing olfaction
and taste 45
1.12 Pheromones and signature mixtures in
humans? 45
1.13 Pollution disrupts chemical communication in
aquatic organisms 45
Summary 46
Further reading 48
2 Methods for identifying and studying
semiochemicals 49
2.1 Bioassays 49
2.2 Collection and analysis of semiochemicals 55
2.3 Using genetic and other techniques from
molecular biology 59
Summary 63
Further reading 63
3 Pheromones, chemical cues, and sexual
selection 65
3.1 Which sex should advertise? 66
3.2 External fertilization and chemical duets 69
3.3 Scramble competition 69
3.4 Pre-copulatory mate guarding 71
3.5 Contests 72
3.6 Mate choice: overview 73
3.7 Mate choice for good genes, mate quality, and
direct benefits 75
3.8 Mate choice for genetic compatibility revealed
by chemical cues 81
3.9 Coolidge effects and rejection of past mates:
been there, done that 86
3.10 Alternative mating strategies 86
3.11 Post-copulatory sexual selection 87
3.12 Sex pheromones and speciation 90
Summary 103
Further r eading 103
4 Coming together and keeping apart:
aggregation pheromones and host-marking
pheromones 105
4.1 Aggregation pheromones and Allee
effects 105
4.2 Host-marking pheromones 110
Summary 112
Further r eading 112
5 Territorial behavior and semiochemicals 113
5.1 Why scent mark on territories? 115
5.2 Scent-fence hypothesis 115
5.3 Scent-matching hypothesis 115
5.4 Border-maintenance hypothesis 120
5.5 Economics of scent-marking patterns in
territories 121
5.6 Dear enemies or nasty neighbors 123
5.7 Counter-marking and over-marking 123
5.8 Scent marking in non-territorial
mammals 124
Summary 125
Further reading 125
6 Semiochemicals and social organization 126
6.1 Colony, kin, family, and individual
recognition 126
6.2 Pheromones and reproduction in social
groups: control or co-operative
signaling? 133
Summary 148
Further reading 148
7 Pheromones and recruitment
communication 150
7.1 Foraging ecology and evolution of recruitment
communication 150
7.2 Social insects as self-organizing systems 160
Summary 164
Further reading 164
8 Fight or flight: alarm pheromones
and cues 165
8.1 Evolution of alarm signals by kin
selection 165
8.2 Subsocial insect families 165
8.3 Alert signals in deer family groups 165
8.4 Clonal sea anemones 167
8.5 Aphids 167
8.6 Social aphids 169
8.7 Termites and social Hymenoptera 169
Summary 172
Further reading 172
9 Perception and response to chemical
communication: from chemosensory receptors
to brains, behavior, and development 173
9.1 How olfaction works: combinatorial
processing of odorants including
pheromones 173
9.2 Evolution of chemoreceptors 188
9.3 The many chemosensory subsystems in
mammals and insects 192
9.4 The overlapping roles and integration of the
accessory and main olfactory systems in
mammals 198
9.5 Pheromones, sex, and brain circuits 201
9.6 Pheromones elicit stereotyped, but modulated,
behavior and/or physiological responses 206
9.7 Pheromone primer effects 209
9.8 Learning of signature mixtures 215
9.9 Interactions between signature mixtures and
pheromones 218
Summary 221
Further reading 222
10 Finding the source: pheromones
and orientation behavior 223
10.1 Investigating orientation behavior
mechanisms 223
10.2 Ranging behavior: search strategies for finding
odor plumes, trails, or gradients 226
10.3 Finding the source: orientation to
pheromones 227
Summary 243
Further reading 243
11 Breaking the code: illicit signalers
and receivers of semiochemicals 244
11.1 Eavesdropping 244
11.2 Chemical communication in mutualisms 249
11.3 Deception by aggressive chemical
mimicry 251
11.4 Social parasites using disguise to escape
detection by social insect hosts 255
Summary 259
Further reading 259
12 Using semiochemicals: applications
of pheromones 260
12.1 Semiochemicals used with beneficial and
domestic animals 260
12.2 Pheromones in pest management 263
12.3 Pest resistance to pheromones? 272
viii
|
Contents
12.4 Commercialization: problems and benefits of
pheromones 272
Summary 273
Further reading 273
13 On the scent of human attraction: human
pheromones? 275
13.1 Olfactory cues to recognition: signature
mixtures 278
13.2 Choosing mates for genetic compatibility:
avoiding kin and going for optimum
difference? 279
13.3 What molecules do humans give off? 284
13.4 Our sense of smell: perception of odors 291
13.5 Human pheromones? 295
13.6 Where next with human pheromones? 301
Summary:To smell is human 302
Further r eading 303
Appendix An introduction to chemical terms for non-
chemists 304
References 312
List of credits 377
Index 378
Contents
|
ix
PREFACE TO THE SECOND EDITION
This book is designed to bring together people already working on chemical communica-
tion and to encourage others, especially chemists (who have a vital role in this research), to
take up the challenge. My aim has been to make an evolutionary understanding of
chemical communication, including pheromones, accessible to a broad scientific and lay
audience.
Pheromone research brings together scientists with many different areas of expertise,
from a rich diversity of chemists to biologists of many kinds. Each area of expertise has its
own jargon and concepts –a behavioral ecologist speaks a different language from a
neuroscientist. The book recognizes that every scientist is a novice outside their own
subject, even science close to their own, so I try to explain ideas in terms understandable by
non-specialists while at the same time aiming to be up to date and detailed enough for the
specialist. I also wanted to write a book that could be enjoyed by the majority of the world’s
scientists whose first language is not English and thus also clearer for everyone.
Pheromones offer exceptional opportunities to study fundamental biological problems.
The rapid progress of the last decades comes from the convergence of powerful techniques
from different areas of science including chemistry and animal behavior, combined with
new techniques in genomics and molecular biology. These allow us to investigate ques-
tions at every level: molecular, neurobiological, hormonal, behavioral, ecological, and
evolutionary. The discoveries from molecular biologists have greatly expanded our
knowledge of the evolutionary biology of olfactory communication. Equally, molecular
biology only makes sense in the context of evolution.
I wrote the first edition to provide the overview of chemical communication we were
then missing, covering the whole animal kingdom, integrating approaches from ecology to
neurobiology, and all with an evolutionary perspective. I have kept the same overall
structure for the book in the new edition. As before, the book is organized around themes
such as sex, speciation, and social organization, rather than taxonomically. The book also
covers the perception and processing of chemosensory information. In each topic I have
aimed to integrate examples from across the animal kingdom. In the same paragraph you
may read about nematodes, moths, snakes, and mice. I explore the often convergent ways
evolved by different kinds of animals to solve the same communication needs.
All chapters have been comprehensively updated and most chapters have been com-
pletely rewritten. The changes are perhaps most significant, as you might expect, in those
parts involving molecular biology, especially in the chapter on perception of pheromones.
Recent results include the surprising discovery that insect chemoreceptors have evolved
independently of vertebrate ones. However, there has also been much new to discuss in
evolution and ecology, including results coming from the application of molecular tech-
niques as well as detailed field work.
Different parts of the book emphasize examples from different taxa. As in the first
edition, mammals feature more strongly than invertebrates in the sections on individual
variation and hormonal effects of pheromones for example, but invertebrates dominate the
sections covering mechanisms of searching behavior.
Chapter 1 defines pheromones and looks at evolution of pheromones as signals. I raise a
pragmatic distinction between pheromones and the chemistry of individual or colony
odors. I also look at the role pheromones play in speciation. The importance of both
common ancestry and convergence in molding chemical signals is a key theme.
Chapter 2 is about the development of analytical tools and how these are changing the
study of chemical communication, allowing us to identify types of molecules previously
hard to work with. New genomics techniques can be used to identify genes involved in
both production and perception of molecules and not just in model organisms such as
Drosophila. On the behavioral side I emphasize the importance of proper randomization of
treatments and “blinding”of experimenters wherever possible. Progress will depend on
productive partnerships between chemists and biologists.
The following six chapters cover different aspects of pheromones in the ecology and
behavior of animals. Chapter 3 is about the evolution of pheromones in sexual selection,
drawing out the many parallels between animals in a wide range of taxa. Among the new
material featured in the chapter is work on Drosophila and moths as well as developments
in evolutionary theory.
Chapter 4 covers Allee effects and the roles pheromones have in spacing organisms,
bringing them together, and keeping them apart.
Chapter 5 reviews territorial behavior, largely in terrestrial vertebrates. The discovery of
the male mouse pheromone, darcin, offers fascinating insights into female mouse behavior
(Roberts et al. 2010, 2012). Darcin prompts her to learn the individual odor of the territorial
male and where the scent mark is.
The parallels between complex social behaviors mediated by chemical communication
in social insects and social mammals are explored in Chapter 6. The queen pheromones of
an increasing number of social insects are being identified. It seems, however, that
mammals do not use pheromones to “suppress”reproduction by subordinate members of
the group.
Recruitment in social insects for foraging and nest building and for defense are covered
by Chapters 7 and 8 respectively. One major change in our understanding is a clearer
distinction between alarm pheromones and cues. The molecules involved in fish alarm are
likely to be cues rather than pheromones.
Chapter 9 explores how olfaction works and how the olfactory receptors themselves
evolve, in enormous variety. Vertebrates and invertebrates are similar in the way they
xii
|
Preface to the second edition
detect and process chemical cues, by combining inputs from neurons carrying different
olfactory receptors, but they achieve this with quite different receptor families, which
evolved independently.
The mechanisms that animals have evolved to find an odor source are discussed in
Chapter 10. We understand more about the mechanisms that fish and birds use than when
the first edition was written. There are some interesting uses of genetically manipulated
Drosophila larvae to explore the ways they orientate in chemical gradients.
Broadcast signals can be eavesdropped. Chapter 11 covers a world of deception and
spying, including new players and a clearer understanding of selection in some classic
examples.
Chapter 12 discusses how an understanding of chemical communication can be used for
agriculture and to control disease vectors. Whereas insects formed the main examples of
pheromone control, pheromones are showing promise for the possible control of vertebrate
pest species, notably the sea lamprey.
Chapter 13 covers the roles of chemical communication in human beings. I discuss the
smells we produce and the ones we can perceive. One of the most surprising things that has
emerged from genomics studies on humans is the enormous variation between us as
individuals in what we can smell. Our olfactory receptor repertoires are individually quite
different: it is likely that we each experience unique olfactory worlds. I conclude the
chapter by exploring some of the limitations of current research on human pheromones
and how we could take it forward.
Finally, the appendix explains the common chemical terminology you will come across.
While some of the molecules important in chemical communication are shown in the
figures, there are too many mentioned in the text to illustrate them all. Instead, you can see
them on sites such as www.chemspider.com, which allows you to search by common name
and shows synonyms as well as the systematic names. Many pheromone molecules,
together with some background, are included on Pherobase www.pherobase.com
(El-Sayed 2013).
Choice of literature for the second edition
This book necessarily offers a selective distillation of an enormous literature. I have
attempted to reflect our consensus understanding of each topic. For reviews, I have
generally used the most recent I could (though I reference earlier reviews if they continue
to be influential). The papers cited have been chosen to reflect both their contributions to
the subject but also because they offer good entry points to the literature (do use
Google Scholar
TM
or Web of Science
TM
to find papers citing these leads). Sometimes you
will findareviewandaparticularexperimental paper both referenced, for example
(Cardé & Haynes 2004; Liénard et al. 2010), which will be obvious, I hope, when you look
Preface to the second edition
|
xiii
them up. The references for this edition are also available at www.cambridge.org/
pheromones.
Wherever possible, I have chosen sources that you will be more likely to be able to find.
Where I have had a choice between equally good papers I have gone for the one in an open
access journal or one that the authors have made available on the web, for example on their
own website. It may be worth searching on an article title to see if it is available. If an
article is not available and you do not have institutional access to the journal, you might
courteously write to the author to see if they have a PDF to send. Most people are pleased to
be asked –I know I am.
Wikipedia
TM
Have you considered helping edit Wikipedia’s entries in our subject? It might seem
surprising for a textbook to recommend its readers to consider contributing their expertise
to Wikipedia, the world’s largest online encyclopedia, but this is where the greatest
influence for our subject will be. As Wikipedia is where most people look first, Bateman
and Logan (2010) encourage scientists to seize the opportunity to make sure that Wikipedia
articles are understandable, scientifically accurate, well sourced, and up to date. Bond
(2011) makes such a call to his fellow ornithologists and presents many advantages of
getting involved. Pheromones and some aspects of chemical communication are briefly
covered in Wikipedia but not to the depth and range of many other areas of science. You
might be able to improve this. Logan et al. (2010) give tips for getting started and guidance
on good practice.
If you would like Microsoft PowerPoint
TM
slides of the illustrations in the book for
teaching or talks, do email me, tristram.wyatt@zoo.ox.ac.uk, letting me know which
chapters’figures you would like.
xiv
|
Preface to the second edition
ACKNOWLEDGMENTS
I would particularly like to thank the following for generously reading the whole book in
draft: Bruce Schulte, Jagan Srinivasan, Joan Wyatt, and Vivian Wyatt. I am also grateful to
many other friends and colleagues for help with various chapters and recent writing
projects, which helped me develop ideas explored in the book, including Olle Anderbrant,
Richard Benton, Thomas Breithaupt, Patrizia d’Ettorre, Monica De Facci, Dick Doty,
Heather Eisthen, Maud Ferrari, Jean-François Ferveur, Kevin Foster, Tom Getty, Stephen
Goodwin, Alan Grafen, Christina Grozinger, Penny Hawken, Matthieu Keller, Jae Kwak,
Jean-Marc Lassance, Darren Logan, Jocelyn Millar, Dan Rittschof, Benoist Schaal, Peter
Sorensen, Számadó Szabolcs, Robert Taylor, Kevin Theis, Martin Thiel,Tobias Uller, Marc
Weissburg, Tom Wenseelers, Danielle Whittaker, Brian Wisenden, and Ben Wyatt.
Any remaining errors are mine of course, and I would welcome comments and sugges-
tions for corrections. You can contact me at tristram.wyatt@zoo.ox.ac.uk.
I would like to thank all the scientists in addition to those listed above who advised me
on their areas of expertise and kindly sent reprints and pre-prints of their work. The book
would not have been possible without their help and generosity. In keeping the range of
animal groups represented as wide as possible, I have had to be selective. Inevitably I have
not been able to include many examples that I would have liked to. I apologise to authors
whose research I was not able to describe here despite its high quality.
Many colleagues generously helped me with high-resolution copies of their illustrations.
I would like to give additional thanks to colleagues who produced new or especially
adapted figures for me, including Christina Grozinger, Harland Patch, Troy Shirangi, Jagan
Srinivasan, and John Terschak.
It is a pleasure to thank Martin Griffiths, Megan Waddington, Abigail Jones, Kath
Pilgrem, Vania Cunha, and other colleagues at Cambridge University Press for their
encouragement and assistance at all stages of producing the second edition.
I would like to thank the publishers and societies listed at the end of the book for
permission to reproduce figures and tables, particularly those which did not charge fees.
SI PREFIXES
Factor Name Symbol
10
–2
centi c
10
–3
milli m
10
–6
micro µ
10
–9
nano n
10
–12
pico p
10
–15
femto f
ABBREVIATIONS
2MB2 2-methyl-but-2-enal
AOB accessory olfactory bulb
AOS accessory olfactory system
BNST bed nucleus of the stria terminalis
cAMP cyclic adenosine monophosphate
cGMP cyclic guanosine monophosphate
CHC cuticular hydrocarbon
CNG cyclic nucleotide-gated channel
CNV copy number variant
cVA cis-vaccenyl acetate
ESP1 exocrine gland-secreting peptide 1
GC gas chromatography
FPR formyl peptide receptor
GABA -aminobutyric acid
GPCR G-protein-coupled receptor
GR gustatory receptor (invertebrates)
GSN gustatory sensory neuron (insects)
GUR gustatory receptor (Caenorhabditis
elegans)
HPLC high-performance liquid chromatography
iGluR ionotropic glutamate receptor
IR ionotropic receptor
JH juvenile hormone
MHC major histocompatibility complex
MGC macroglomerular complex
MOB main olfactory bulb or OB
MOE main olfactory epithelium
MOS main olfactory system
MOT medial olfactory tract
MTMT (methylthio)methanethiol
MUP major urinary protein
MPOA medial pre-optic hypothalamus
OB olfactory bulb (MOB)
OR olfactory receptor
ORCO olfactory receptor coreceptor (insects)
OSN olfactory sensory neuron (also termed
olfactory receptor neuron, ORN)
SEM scanning electron micrograph
SEM standard error of the mean
SNP single nucleotide polymorphism
SPME solid phase micro extraction
T1R taste receptor type 1
T2R taste receptor type 2
TAAR trace amine-associated receptor
TRC taste receptor cell
TRPC2 transient receptor potential channel
2 (= TRP2)
V1R vomeronasal receptor type 1
V2R vomeronasal receptor type 2
VNO vomeronasal organ
VNS vomeronasal system (= accessory olfactory
system)
1Animals in a chemical world
When two dogs meet and sniff, they gain a wealth of
information from each other’s smells. Each dog will dis-
cover the sex, maturity, and hormonal state of the other;
some of these smells will be species-wide dog phero-
mone signals. Each dog also detects the individual smell
of the other, which it learns as a “signature mixture”to
remember in case they meet again.
When two ants meet and sweep antennae over each
other, they have an olfactory exchange of information
similar to that of the dogs, discovering age, sex, ovarian
stage (reproductive or not), and caste (worker, soldier,
queen), all signals from species-wide pheromones. They
also detect the colony odor of the other ant, enabling
them to decide by the “signature mixture”whether the
other ant is a nestmate or not.
All animals produce a chemical profile, present on the
body surface, released as volatile molecules, and from
scent marks that they deposit (by dogs on lamp-posts for
example) (Figures 1.1, 1.2, 13.2). As chemical senses are
ancient and widespread, shared by all organisms
including bacteria, animals are pre-adapted to detect
chemical information in the environment (Box 1.1).
Across the animal kingdom, animals of all kinds gain
chemosensory information from other organisms.
Chemical senses are used to locate potential food sour-
ces and detect predators. Chemical senses also mediate
the social interactions that form the focus of this book,
as illustrated by the dogs and ants above. We can prob-
ably say that more organisms use chemosensory com-
munication than any other mode.
A chemical involved in the chemical interaction
between organisms is called a semiochemical (Box 1.2).
Some of the semiochemicals emitted by animals are
pheromones, evolved as signals for communication.
Other semiochemicals, such as the carbon dioxide in
exhaled breath, did not evolve as a signal, but can be
exploited as a cue by blood-sucking mosquitoes as a way
of finding a host. Some of the othermolecules emitted by
animals, such as odors due to infections, may also be
cues. The distinction between signals and cues is explored
further in Section 1.3.
Pheromones and signature mixtures are semiochemi-
cals used within a species. Semiochemicals acting
between individuals from different species are called
allelochemicals and are further divided depending on
the costs and benefits to signaler and receiver (Box 1.2)
(Chapter 11) (Nordlund & Lewis 1976; Wyatt
2011). Pheromone signals can be eavesdropped (“over-
heard”) by unintended recipients: for example, specialist
predatory beetles use the pheromones of their bark bee-
tle prey to locate them. The predators are using the bark
beetle pheromones as kairomones. Animals of one
species can emit fake, counterfeit signals that benefit
themselves at the cost of the receiving species. Chemical
signals used in such deceit or propaganda are termed
allomones: for example, bolas spiders synthesize partic-
ular moth pheromones to lure male moths of those spe-
cies. Semiochemicals benefiting both signaler and
receiver in mutualisms, such as those between sea ane-
mones and anemone clownfish, are termed synomones.
The multiplicity of terms is only useful as shorthand and
the terms are clearly overlapping, not mutually exclusive
(for example, a molecule used as a pheromone within a
species can be used as a kairomone by its predator).
My aim in this book is to focus on patterns across the
animal kingdom. I have tried to include examples from as
many animal taxa as space allows, but for more detail see
the suggestions in further reading and references in the
text. This chapter introduces the ways in which animals
use semiochemicals and many of the topics are explored
at greater length in later chapters (see Preface for over-
view and rationale).
1.1 Intra-specific semiochemicals:
pheromones and signature mixtures
Modern pheromone research could be said to date from
1959, when the chemist Adolf Butenandt and his team
identified the first pheromone, the silk moth’s sex
pheromone bombykol, which prompted the coining of
the word “pheromone,”from the Greek pherein,to
transfer; hormo¯n, to excite (Butenandt et al. 1959;
Karlson & Lüscher 1959). Butenandt’s discovery
established that chemical signals between animals
exist and can be identified (Chapter 2). From the start,
Karlson and Lüscher (1959) anticipated pheromones
would be used by every kind of animal, from insects
and crustaceans to fish and mammals. Since then,
pheromones have been found across the animal king-
dom, in every habitat on land and underwater, carry-
ing messages between courting lobsters, alarmed
aphids, suckling rabbit pups, mound-building ter-
mites, and trail-following ants (Wyatt 2009). They are
also used by algae, yeast, ciliates, and bacteria. It is
likely that the majority of species across the animal
kingdom use them for communication of various
kinds. Much is known about the pheromones of
Chemical profile
Made up from many sources, e.g.
•
e.g.
peptides
by HPLC
small molecule size large
e.g.
hydro-
carbons
by GC
• secretions
• immune system
• hormones
• bacterial symbionts
• diet
• other conspecifics
• collected from flowers
• infections
Pheromone 1
Pheromone 2
Pheromone 3
Signature mixture A
Signature mixture B
•••
•••
•••
•••
•••
•••
Figure 1.1 Pheromones occur in a background of molecules
that make up the chemical profile consisting of all the mol-
ecules extractable from an individual. The chemical profile
(top) is an imaginary trace from an imaginary column capa-
ble of analyzing all the molecules (at one side is high-
performance liquid chromatography (HPLC) with large pro-
teins, at the other is gas chromatography (GC) with small
volatile molecules). Each peak represents at least one
molecule.
Much of the chemical profile is highly variable from indi-
vidual to individual. The sources of the molecules in the
chemical profile include the animal itself as well as its envi-
ronment, food, bacteria, and other individuals etc. It is this
complex background that makes identifying pheromones so
challenging in many organisms.
The pheromones could include sex pheromones or ones
related to life stage or caste. The pheromones would be the
same in all individuals of the same type in a species (domi-
nant male, worker ant, forager, etc.); that is, they are anony-
mous, common across the species. As examples, I have
included some possible kinds of pheromones that are
known from organisms (not necessarily in the same species):
aspecific combination of large and small molecules
(Pheromone 1), a combination of small molecules
Figure 1.1 (cont.)
(Pheromone 2), or a particular large molecule by itself
such as a peptide (Pheromone 3).
The signature mixtures (A and B) are subsets of variable
molecules from the chemical profile that are learned as a tem-
plate for distinguishing individuals or colonies. Different
receivers might learn different signature mixtures of the same
individual. For example, a male might learn a different signa-
ture mixture of his mate than the one her offspring might learn.
Hypothetically it is conceivable that the male might learn dif-
ferentsignaturemixturesforthesamefemaleindifferentcon-
texts, say immune-system associated molecules in one context
and more diet influenced molecules in another. In other words,
signaturemixturesseemtobea“receiver-side”concept.
Adapted from Wyatt (2010). The layout is inspired by
Figure 1 of Schaal (2009).
2
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Animals in a chemical world
insects, fish, and mammals, but some other taxa have
not been well studied. For example, crabs and other
Crustacea make extensive use of pheromones but
relatively few of these have been chemically identified
(Breithaupt & Thiel 2011). Birds, too, have now been
shown to have a rich olfactory life though we are only
(a)
(b)
(d)
mated alpha
1400
1200
1000
FID (mV)
0
1000
1200
1400
1600
1800
older sterile
worker
2000
10 20 30 min
1218
27–29
35–38 46–48
40
42–45
54
56–59
60–
63
67–70
71–74
77
78
79–81
*
*
(c) 9
9-hentriacontene
Figure 1.2 The “queenless”ant, Dinoponera quadriceps, lives in small groups headed by an alpha female, the only egg-laying
individual in the colony. The hierarchy is maintained by physical aggression. This can include gaster rubbing (a) in which the
alpha female rubs the antenna of the subordinate on the cuticular hydrocarbons, which include the alpha’s pheromone “badge”
of dominance, 9-hentriacontene (c, top). This molecule is characteristic of alpha females in all colonies of the species.
(b) If a subordinate female becomes reproductive and starts to produce the molecules characteristic of an alpha female, other
ants in the colony detect this and immobilize her (an example of an honest signal maintained by punishment, Section 1.6).
(c) The colony profile of ants in the colony can be shown in a solid phase micro extraction (SPME) gas chromatographic
analysis of their cuticular hydrocarbons (Monnin et al. 1998) (Chapter 2). As well as the many-peaked hydrocarbon chemical
profile shared by the other ants in the colony, the alpha female also has the additional peak #40 (indicated by the asterisk) which
is the pheromone 9-hentriacontene. Below, her fellow colony members have the same colony profile as her but lack this peak.
(d) Non-destructive SPME sampling allowed changes in the percentage of 9-hentriacontene in the cuticular hydrocarbons of
an individual ant to be followed in the days after she became the alpha female. In a larger sample of ants undergoing the
transition, the significant difference was between the quantities at 15 and 30 days.
(a) and (b) from Monnin and Peeters (1999), (c) chromatograph from Monnin et al. (1998), (d) from Peeters et al. (1999).
1.1 Intra-specific semiochemicals
|
3
Box 1.1 Chemical and other senses compared
Chemical senses are shared by all organisms including bacteria. However, while the general way
that molecules interact with chemosensory receptor proteins in a “lock and key”manner is
shared, the chemosensory receptor proteins are highly variable across the animal kingdom and
even within animal taxa. This is because the chemosensory system, like the immune system,
tracks a changing world of molecules generated by other organisms. Over evolutionary time, the
chemosensory systems of organisms co-opt, test, and discard chemosensory receptor genes and
neural coding strategies, leading to great divergences in receptors (Bargmann 2006b;
Bendesky & Bargmann 2011). Chemosensory receptor genes turn over rapidly, in a birth-and-
death process of gene duplication and loss (see Chapter 9). The rapid evolution of chemosensory
receptor proteins, evolved independently in insects and vertebrates, made chemoreception much
harder to investigate than vision (Chapter 9). The key proteins (opsins) for light-detection in eyes
do vary considerably and insect and vertebrate opsins have diverged. However, unlike chemo-
sensory receptor proteins, they form a large monophyletic group within the G-protein-coupled
receptor (GPCR) superfamily (Porter et al. 2012).
At the level of the individual, variation in olfaction is much greater than in the opsin genes.
For humans, mutations in the four genes for opsin receptor proteins sensitive to different
wavelengths of light give us a small number of different kinds of color vision deficiency or
“color blindness.”By contrast, we have more than 400 olfactory receptor genes, each of which
can be mutated, so each of us smells a unique world (Chapter 13) (Olender et al. 2012). For this
reason too, we might each remember different mixtures of molecules as signature mixtures to
recognize the odors of other people.
The chemical senses of olfaction and taste are very different from vision and hearing, which
detect the energy of different wavelengths in the form of light and sound: chemical senses rely on
the physical movement of molecules from the signaler to the sense organ of the receiving animal.
This requires either diffusion, only likely to be important for small organisms at the scale of
millimeters, or flow of currents (Chapter 10). Either way, the time taken for molecules to travel to
the receiver means that chemical signals are rarely instantaneous in the way that visual and
acoustic signals can be.
Challenges remain for studying chemical communication (Chapter 2). We can record and play
back the sound signals of an animal easily enough, but we do not have devices to do the same for
chemical signals. Each molecule needs to be correctly synthesized, in every detail (see
Section 1.4.3 and Appendix), before it can be “played back”to the animal. This can be
challenging for a team of biologists and makes chemist partners invaluable. For example,
methyl-branched alkanes, important components of ant CHCs, are not commercially available
and synthesizing these is a costly and time-consuming process (van Zweden & d’Ettorre 2010).
Yet, perhaps more than other modalities such as sound or vision, chemosensory systems are
amenable to molecular manipulation: in model systems we can now study communication at the
4
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Animals in a chemical world
just beginning to discover what molecules their pher-
omones might be (Campagna et al. 2012; Caro &
Balthazart 2010; Hagelin & Jones 2007; Zhang et al.
2010). Research on human semiochemicals is at a
similarly early stage; I review our current state of
knowledge in Chapter 13.
The idea of chemical communication was not new in
1959. The ancient Greeks knew that the secretions of a
female dog attracted males. Charles Butler
(1623) warned in The Feminine Monarchie that if a
beekeeper accidentally crushes a honeybee, the bees
“presently finding it by the ranke smell of the poison-
ous humor, will be so angry, that he shall have work
enough to defend himself.”In The Descent of Man, and
Selection in Relation to Sex (1871), Charles Darwin
included chemical signals alongside visual and audi-
tory signals as outcomes of sexual selection, describ-
ing the strong smells of breeding males in moths,
pythons, crocodiles, musk ducks, goats, and elephants.
Jean-Henri Fabre (1911), also writing in the 1870s,
described how male great peacock moths, Saturnia
pyri,flocked around a female moth hidden behind
wire-gauze, but ignored visible females sealed under
glass. A female moth’s smell could be collected on a
cloth and males would flock to that too. Many other
scientists in the nineteenth century and first half of the
twentieth century, including Niko Tinbergen, had
worked on phenomena we would recognize as being
mediated by pheromones (some are mentioned in
Karlson & Lüscher 1959). However, because the
quantities emitted by an individual animal were so
small, the chemistry of the day could not identify
them, until the inspired idea of using domesticated silk
moths, which could be reared in the hundreds of
thousands necessary to collect enough material for
analysis using the techniques available at that time
(Chapter 2).
The enormous variety of organic molecules identi-
fied as pheromones since the first, bombykol, in 1959
is as diverse as the animal kingdom, and offers an
ongoing challenge for chemists interested in the
identification, synthesis, and exploration of natural
functions of novel compounds (Cummins & Bowie
2012; El-Sayed 2013; Francke & Schulz 2010). The
likely explanation for the diversity of pheromone
chemistry is that these signals have evolved from
chemical cues naturally released by organisms, facili-
tated by the broad tuning of olfactory receptors
(Chapter 9) (Section 1.3).
Invertebrates and vertebrates, in a wide range of
habitats, use chemical communication in similar ways.
Animals as different as moths and elephants may share
the same molecule(s) as part of their pheromones.
However, there are more fundamental parallels in
sensory processes, even if we are not always sure
whether this has occurred by convergence or via
shared ancestors. The parallels include the combina-
torial way that the sense of smell is organized in the
brain: olfactory sensory neurons with the same olfac-
tory receptor all collect at the same spot (glomerulus)
in the brain; the information from different glomeruli
is combined to identify the molecule (the combinato-
rial mechanism) (Chapter 9).
1.1.1 Pheromones
Pheromones are molecules that have evolved as a
signal between organisms of the same species. The
Box 1.1 (cont.)
level of the genes involved in signal production (e.g., enzyme pathways) and signal reception
(genetics of receptors, brain, and behavior) especially in model animals such as Caenorhabditis
elegans, moths, Drosophila, and the mouse.
1.1 Intra-specific semiochemicals
|
5
signal elicits a specific reaction, for example, a
stereotyped behavior (releaser effect) and/or a
developmental process (primer effect) from a conspe-
cific (member of the same species) (Box 1.2)
(Section 1.9) (Wyatt 2010). Many, probably most,
pheromones (including the sex pheromones of most
moths and some mammal pheromones) are not single
compounds, but rather a species-specific combination
of molecules in a precise ratio. This combination is the
pheromone (though sometimes called a multicompo-
nent pheromone or pheromone blend). A pheromone
can elicit a variety of effects, depending on the context
and the receiver (Section 1.8). Responses to phero-
mones usually seem to be innate (though this is not a
part of the definition). In the few instances where
learning is first required for a pheromone to act, all
animals normally learn the same molecule(s), which is
what defines it as a pheromone (Section 1.2).
Box 1.2 Definitions of chemical mediators
Pheromones are signals. The other categories of semiochemicals in this box are cues that can be
used for information but did not evolve for that function (Section 1.3). Adapted from Wyatt
(2010, 2011) based on Nordlund and Lewis (1976).
See Wyatt (2011) for a discussion of the origins and usage of these terms. I discuss inter-
specific interactions mediated by allelochemicals in Chapter 11. “Infochemical”as an alter-
native to “semiochemical”was proposed by Dicke and Sabelis (1988) though its main change
was to replace “produced or acquired by”with “pertinent to biology of”in each case for
allelochemicals.
A. Hormone: a chemical agent, produced by tissue or endocrine glands, that controls various
physiological processes within an organism. (Nordlund & Lewis 1976).
B. Semiochemical: a chemical involved in the chemical interaction between organisms.
(Nordlund & Lewis 1976) (from the Greek: semeion, mark or signal).
1. Pheromone: molecules that are evolved signals, in defined ratios in the case of multiple
component pheromones, which are emitted by an individual and received by a second
individual of the same species, in which they cause a specific reaction, for example, a
stereotyped behavior or a developmental process. (Wyatt 2010, modified after Karlson and
Lüscher 1959). (From the Greek: pherein, to carry or transfer, and hormo¯n, to excite or
stimulate).
2. Signature mixture: a variable chemical mixture (a subset of the molecules in an animal’s
chemical profile) learned by other conspecifics and used to recognize an animal as an
individual (e.g., lobsters, mice) or as a member of a particular social group such as a family,
clan, or colony (e.g., ants, bees, badgers). (Wyatt 2010; derived from Johnston’s“mosaic
signal”sensu 2003, 2005; Hölldobler and Carlin’s, 1987 ideas; and Wyatt’s, 2005 “sig-
nature odor”).
3. Allelochemical: chemical significant to organisms of a species different from their source,
for reasons other than food as such. (Nordlund & Lewis 1976).
6
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Animals in a chemical world
Karlson and Lüscher (1959) predicted that most
pheromones would act via the conventional senses of
olfaction or taste, but that some pheromones might be
ingested and act directly on the brain or other tissues.
We would call these allohormone pheromones
(Section 1.11). They speculated that royal jelly in hon-
eybees might contain such a pheromone, and indeed an
active molecule (royalactin) has been identified, which
causes larvae receiving it to develop into queens rather
than workers (Chapter 9) (Kamakura 2011).
Pheromones include the familiar sex attractant
pheromones, and numerous others that serve a wide
variety of functions. Some pheromones are specificto
different life stages or castes. One key feature of
pheromones is that they are “anonymous,”that is, a
given pheromone is the same in all individuals within a
species of the same type (e.g., male or female) or
physiological state, and it conveys a stereotyped mes-
sage that is independent of the individual producing it
(Hölldobler & Carlin 1987).
However, quantities of pheromone can differ
between individuals or in the same individual over
time. Some male mouse pheromones, the farnesenes,
are produced only by dominant male territory holders,
not subordinates (Hurst & Beynon 2004). In the ant
Dinoponera quadriceps, when an ant becomes the top
(alpha) female, she starts to produce the standard
chemical badge of a “top female”in her species, 9-
hentriacontene (Figure 1.2) (Peeters et al. 1999).
However, in the male mouse and the top female ant of
these examples, the pheromones are still anonymous
(Hölldobler & Carlin 1987; Hölldobler & Wilson 2009,
p. 270). They indicate the presence of, for example, a
dominant male mouse or an alpha female ant, not a
particular individual.
Some of our expectations of pheromones have been
heavily influenced by the well studied response of
male moths to the sex attractant pheromones of con-
specific females. For example, the antennae of male
moths have thousands of highly specialized receptors
Box 1.2 (cont.)
Pheromones
species-wide signals
Signature
mixtures
learned by
receiver from
highly variable
chemical profile of
conspecific
Semiochemicals
Between members of
same species
Allelochemicals
Between members of
different species
Allomones
benefit emitter, of
a different species
Kairomones
benefit receiver, of
a different species
Synomones
benefit both emitter &
receiver, of different
species
Diagram showing the relationships between different kinds of semiochemicals. Inspired by Box 7.1 in de Brito-
Sanchez et al. (2008) and other sources.
1.1 Intra-specific semiochemicals
|
7
for the pheromone and specificareasofthebrain
dedicated to processing the pheromonal signal.
However, other pheromone processing in insects may
involve less specific receptors, without dedicated
brain areas (glomeruli) (see Chapter 9). Thus, we now
know that narrowly tuned and highly specialized
receptors and dedicated glomeruli are not a prereq-
uisite for pheromone use. For example, honeybee
alarm pheromone components seem to be processed
by receptors and glomeruli that also process other,
non-pheromone molecules (Chapter 9) (Wang et al.
2008b).
Similarly, male moths’enormously enlarged anten-
nae, covered with thousands of olfactory sensilla that
are tuned specifically to the pheromone, reflect selec-
tion for extreme sensitivity to low concentrations of
female pheromone, necessitated by the scramble com-
petition to be the first to reach the female (Chapters 3, 9,
and 10). Based on the great body of work on male
moths, we tend to expect all receivers of pheromones to
be very sensitive to them and to respond at great dis-
tances. However, other animals may not use attractant
pheromones at all, although they may still use sex-
specific contact pheromones for sex and species recog-
nition when in close proximity to each other (for
example the contact sex pheromones used by some
copepods; Snell 2011b). The stimulus concentration on
contact can be high and thus exquisite sensitivity in the
olfactory or gustatory receptors that perceive contact
pheromones is unnecessary. A small number of speci-
alized chemosensory neurons may be sufficient. This
seems to be the case for short range species recognition
mediated by contact chemicals during the courtship of
Drosophila males and females (Chapters 3 and 9).
When the original definition of pheromone was
proposed in 1959, only a single pheromone had been
chemically identified: bombykol of the silk moth
female (Karlson & Lüscher 1959). It is a tribute to
Karlson and Lüscher, and their wide consultation, that
the definition has held up so well (Wyatt 2009). It is not
surprising that the definition has needed to be updated
slightly since then (Box 1.2) (Wyatt 2010). (See Box 1.3
and Box 1.4 for why words matter and how distin-
guishing the concepts can be helpful).
Box 1.3 Pheromones and signature mixtures: why words matter
Definitionsmatter because they can provide useful generalizations and predictions. My purpose in
separating pheromones from signature mixtures is pragmatic and based on the heuristic (rule of
thumb) value of separating these kinds of chemical information. When we say something is a
pheromone,the reader can anticipate that it isa molecule (or a particular combination and ratio of
molecules for a multicomponent pheromone) that will be found, for example, in all sexually
mature females. Quantities of the pheromone may differ between individuals, and this may be
important in mate choice (Chapter 3), but not in ways that allow an individual female to be
recognized as an individual. In Hölldobler and Carlin’s (1987) terms, the pheromone signal is
“anonymous,”it could beany female (see also Hölldobler & Wilson 2009, p. 270). (See also Box 1.4
Operational definition of pheromone.)
In contrast, if a phenomenon, such as a male distinguishing his mate from other females, relies
on a learned signature mixture, it would be fruitless to search for a single combination of
molecules eliciting individual mate recognition across the species: it is precisely the great
8
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Animals in a chemical world
Box 1.3 (cont.)
differences between females’chemical profiles that makes learning signature mixtures by males
possible.
In the first edition of this book, I included signature mixtures within the definition of
“pheromones”(Wyatt 2003, pp. 2–4). I now think it is more helpful to explicitly separate
signature mixtures as it is emerging that their characteristics are different, in particular the
variability of signature mixtures and the need for learning (Tables 1.1 and 1.2) (Wyatt 2010). It
seems to be a useful distinction, which has helped understand phenomena best explained by
species-specific pheromone molecules appearing on a background of variable chemical profiles
from which signature mixtures are learned, in situations as varied as the male effect in sheep
(Hawken & Martin 2012) and trail pheromones in stingless bees (Reichle et al. 2013).
So, to be clear, not all molecules included in this book are pheromones. I will discuss many
molecules that are not pheromones (Section 1.3), including the highly variable signature
mixtures used to avoid mating with kin (Chapter 3) and learned by ants to distinguish nestmates
from non-nestmates (Chapter 6), as well as chemical cues such as barnacle settlement cues
(Chapter 4) and fish alarm cues (Chapter 8).
Box 1.4 Operational definition of pheromone
The formal definition of a pheromone includes both evolved emission and reception of the signal
for that function (Section 1.3) (Table 1.1) (Maynard Smith & Harper 2003, p. 3). However, for
many otherwise respectable pheromones, we do not know enough about the ways in which
production and/or reception may have evolved. So, I propose we formalize an operational
definition of pheromone, which most people already use in practice, as “fully identified mole-
cule(s), the same across a species, in all lactating mature females for example, which when
synthesized elicit the same characteristic response in the conspecific receiver as the natural
stimulus.”
To legitimately assert that a molecule or specific combination of molecules qualifies as a
pheromone for a species (or in a genetically defined subpopulation within a species):
1. The synthesized molecule/combination of molecules (combination) should elicit the same
response as the natural stimulus in the bioassay.
2. It should act in this way at realistic concentrations similar to the natural stimulus.
1.1 Intra-specific semiochemicals
|
9
1.1.2 Signature mixtures
Returning to the dogs and ants that opened this chap-
ter, the individually distinctive mixture of molecules
that allows dogs to tell each other apart by smell and
allows ants, at a colony level, to distinguish nestmate
from non-nestmate, are not pheromones and were
not included in the original definition.
We need a different term for the molecules that
animals learn and use to distinguish other individuals
or colonies. I have proposed “signature mixture”
(Wyatt (2010) inspired by Johnston’s (2003, 2005)
“mosaic signal,”Hölldobler and Carlin’s (1987) ideas,
and based on Wyatt’s (2005) “signature odor”). I think
some of the early doubts about mammal pheromones
(Box 1.5) came from treating signature mixtures as if
they were pheromones. Be aware when reading the
past and current literature that the term “pheromone”
is still used ambiguously and may be used in contexts
where “signature mixture”or “chemosensory cues”
would be more accurate or helpful.
Signature mixtures are the subsets of variable mol-
ecules from the chemical profile of an individual
(Figure 1.1) that are learned as templates by members
of the same species (conspecifics) and used to recog-
nize an organism as an individual or as a member of a
particular social group such as a family, clan, or colony
Box 1.4 (cont.)
3. For multicomponent pheromones, experiments should demonstrate that all compounds in
the combination are necessary and sufficient.
4. Only this molecule or the proposed combination of molecules elicits the effect (and other
similar molecules or combinations that the animal would encounter do not).
5. There should be a credible pathway for the pheromone signal to have evolved by direct or
kin selection.
6. Quantities may vary between individuals (e.g., subordinate and dominant males).
The requirements follow those explored in Chapter 2. They are the equivalent of “Koch’s
postulates”for establishing causal relationships for pheromones: initial demonstration of an
effect mediated by a pheromone, then identification and synthesis of the bioactive molecule(s),
followed by bioassay confirmation of activity of the synthesized molecules. It can be equally
important to show that other similar molecules do not have the effect of the proposed
pheromone.
How the response develops (ontogeny) in an individual is a separate question (Section 1.2).
Normally we do not know the details. Fish alarm substances are thought to be cues rather than
pheromones (Chapter 8) as they fail to satisfy criterion #5.
Sadly, the experimental literature on humans, and other mammals, includes many unidenti-
fied extracts or molecules that have never been rigorously demonstrated to be biologically active
by the full bioassay evidence and synthesis process. It is misleading to call them even “putative
pheromones”(Chapter 13).
10
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Animals in a chemical world
Box 1.5 Mammal pheromones
There is good evidence that mammals have pheromones that fit well with the original definition
(Brennan & Zufall 2006; Wyatt 2010), despite doubts from some authors (Beauchamp et al. 1976;
Doty 2010). The many small-molecule mammal pheromones include the rabbit mammary
pheromone 2-methylbut-2-enal (2MB2) (Schaal et al. 2003) (see below), male mouse pheromones
such as (methylthio)methanethiol (MTMT) (Lin et al. 2005), trimethylamine (Li et al. 2013),
dehydro-exo-brevicomin and 2-sec-butyl-4,5-dihydrothiazole (Novotny 2003; Novotny et al.
1985), and Asian elephant pheromones including frontalin (1,5-dimethyl-6,8-dioxabicyclo
[3.2.1]octane) and (Z)-7-dodecen-1-yl acetate (Rasmussen et al. 2003). Many of these molecules
(or ones similar) are also used as pheromones by insects (Section 1.4.1) (Table 1.2). As well as
small-molecule pheromones, mammals also have large-molecule pheromones, such as, in mice,
exocrine gland-secreting peptide 1 (ESP1) (Haga et al. 2010) and the protein pheromone darcin
(Chapter 9) (Roberts et al. 2010, 2012). See Figure 9.7 for some of the large and small molecules
used by mice.
Part of the reason for the earlier doubts was confusion between pheromones and the highly
variable chemical profiles of mammals (for example, see Figure 13.2). In addition, over the years,
expectations about pheromones in mammals have built up, perhaps based on misconceptions
about insect pheromones (e.g., Doty 2010): contrary to these expectations, as shown in a variety
of animals including insects, pheromones do not have to be unique species-specific molecules
(Section 1.4.1), animals’responses to pheromones can vary (Section 1.8), and pheromones can
involve elements of learning (Section 1.2).
A separate set of problems came from some scientists in the 1990s onwards, using mice as
a model system to study mammal pheromones, who seemed to assume, despite earlier
evidence to the contrary, that (a) pheromones would be exclusively detected by the VNO
system, and that (b) all molecules detected by the VNO were pheromones (Baxi et al. 2006;
Wyatt 2009). As explored in Chapter 9, it is now confirmed that (i) pheromones are detected
by both the VNO and the main olfactory system, depending on species and pheromone, (ii)
that the VNO also responds to other odorants, and (iii) that there is extensive integration of
inputs from the two olfactory systems.
An example of a small-molecule pheromone perceived by the main olfactory system is the
rabbit mammary pheromone, 2MB2, which stimulates rabbit pups to suckle (Charra et al.
2012; Schaal et al. 2003). The pups respond to pheromone from their mother’s nipple region,
which elicits stereotyped searching, usually successful in just six seconds. The pheromone
also prompts the pups to learn their mother’s signature mixture (Coureaud et al. 2010). Newly
born humans use olfactory stimuli, possibly including a pheromone, to find their mother’s
nipple (Chapter 13) (Doucet et al. 2009, 2012).
1.1 Intra-specific semiochemicals
|
11
Box 1.5 (cont.)
(a)
(c)
(b)
60
1,000 1,200 1,400
Retention index
1,600 1,800
40
20
Responding pups (%) FID signal (a.u.)
Hexan-2-one
Heptan-2-one
Decan-2-one
Dec-2-enal
Undec-2-enal
Butanoic acid
Butyrolactone
Decanal
Benzaldehyde
D,L-Limonene
Cyclopentanone
Cyclohexanone
Oct-1-en-3-one
Pyridine
Octanal
2-Methylbut-2-enal
2-Methylbutan-1-ol
2-Ethylhexan-1-ol
2-Methylpropan-1-ol
2-Methylcyclopentan-1-one
Butan-1-ol
(d) 100
80
60
40
20
0
Responding pups (%)
Hexan-2-one (40)
Heptan-2-one (15)
Decan-2-one (15)
Dec-2-enal (15)
Undec-2-enal (15)
Butanoic acid (15)
Butyrolactone (20)
Decanal (15)
Benzaldehyde (35)
D,L-Limonene (15)
Cyclopentanone (15)
Cyclohexanone (15)
Oct-1-en-3-one (15)
Pyridine (20)
Octanal (15)
2-Methylbut-2-enal (40)
2-Methylbutan-1-ol (40)
2-Ethylhexan-1-ol (15)
2-Methylpropan-1-ol (40)
2
-Methylcyclopentan-1-one (15)
Butan-1-ol (40)
12
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Animals in a chemical world
(Box 1.2). “Signature”is used as it denotes
individuality.
The signature mixture is the mixture of molecules
(and likely, their relative ratios) that are learned. The
template is the neural representation of the signature
mixture stored in the memory of the learner (after van
Zweden & d’Ettorre 2010).
There are two distinguishing characteristics of
signature mixtures: first, a requirement for learning
and, second, the variability of the cues learned,
allowing other individuals to be distinguished by
their different chemical profiles (see Section 1.7 for a
more detailed explanation). Other comparisons
between pheromones and signature mixtures are
explored in Table 1.1.
The signature mixture molecules in the chemical
profile, learned by receivers as the template for
recognition, can be produced by the organism itself,
acquired from the diet, shared local environment, or
other organisms (Section 1.7). In ants, the chemical
profile may have species-characteristic types of
molecules, but each colony produces different com-
binations and ratios of these (van Zweden &
d’Ettorre 2010). For example, different colonies of
the ant Formica exsecta have different colony-
specific combinations of various (Z)-9-alkenes,
under genetic influence (Martin & Drijfhout 2009b;
Martin et al. 2008c). What makes this different from
a pheromone is that each colony has a different set
of ratios of these shared molecules –it is what
allows the colonies to be distinguished. By contrast
a multicomponent pheromone would be expected to
have a uniform ratio across a population, the same
in each colony.
Different receivers might learn different combina-
tions of molecules from an individual’s profile as the
Box 1.5 (cont.)
(Figure facing). The discovery of the rabbit mammary pheromone, 2-methylbut-2-enal (2MB2), used a
linked gas chromatograph-olfactory (GCO) assay, which allowed concurrent detection by neonatal
rabbits and by a flame ionization detector (FID) (Chapter 2). (a) Photographs show the sequence (duration
5 s) of a two-day-old pup’ssearching–grasping response directed to the glass funnel of the GC sniff-port.
(b) Typical chromatogram of rabbit milk effluvium (upper panel) and concurrent percentage of pups
responding with searching–grasping responses (lower panel; inverted scale). The regions of the chromato-
gram eliciting more than 20% of responses (summed across 25 GCO runs) and the compounds eluting in
these regions are shown. (c) Screening, by presenting a glass-rod, of milk volatiles presumed to have
behavioral activity: two-day-old pup at rest (left) and exhibiting grasping (right) to a glass rod carrying
2MB2. (d) Frequency of searching (open bars) and seizing (solid bars) directed to the glass rod carrying one
of the 21 compounds identified in milk. Numbers in parentheses indicate the numbers of pups tested.
(Schaal et al. 2003).
The only significant mammal group for which chemical communication has not been dem-
onstrated are whales and dolphins (cetaceans). However, it is possible and may be discovered in
future, as baleen (mysticete) whales have a good olfactory system, which they may also use to
detect upwind concentrations of plankton by smell (as albatross do, Chapter 10) (Thewissen et al.
2011). Some baleen whales have a Harderian gland, which in some rodents produces phero-
mones, though it may have other functions (Funasaka et al. 2010).
1.1 Intra-specific semiochemicals
|
13
Table 1.1 Contrasting pheromones with signature mixtures. Hölldobler and Carlin (1987) introduced the idea of
anonymous signals (pheromones) contrasted with variable signature mixtures (though their terminology was
different) (see also Hölldobler & Wilson 2009, p. 270). The anonymous pheromone signals are uniform
throughout a category (e.g., species, male, female, and perhaps molt state and dominance status). In contrast,
signature mixtures vary between individuals or colonies and can be used to recognize the organism as an
individual or member of a particular social group such as a family or colony. From Wyatt (2010).
Pheromone Signature mixture
Stimulus A species-wide molecule (or particular
defined combination of molecules).
A combination of molecules, never a sin-
gle molecule. Combination of molecules
varies between individuals or colonies.
Possible “receiver side effect”: there may
not be one signature mixture for each
individual, as different conspecifics
(receivers) may learn different subsets of
molecules in the individual’s chemical
profile (Figure 1.2).
Type of
information
Anonymous (independent of the source
individual).
Variable (allows recognition of an indi-
vidual or group such as a colony).
Molecule size Any size or type, depending on habitat,
medium, signal duration, and phylogeny.
Any size or type, depending on habitat,
medium, signal duration, and phylogeny.
Source Make self or acquire/modify. Usually
genetically based.
Make self or acquire/modify. Use chemical
mixtures, genetically based or from the
environment or a combination.
Learning Little requirement for learning of the signal
molecule(s).
Innate, stereotyped, or hardwired (with the
caveat of developmental constraints).
Cues learned.
Response Elicits a stereotyped behavior and/or
physiological response. May be context
dependent.
Learned and can be used to distinguish
individuals or groups (can lead to stereo-
typed response e.g., aggression). May be
context dependent.
Olfactory receptor
proteins
Some (e.g., moth sex pheromones) have
high specificity olfactory receptor proteins
(and the “labeled lines”and “dedicated
glomeruli”that result). Many other phero-
mones do not.
Low specificity, broadly tuned receptors.
14
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Animals in a chemical world
signature mixture to recognize that individual (see
legend to Figure 1.1). In other words, signature mix-
tures seem to be a “receiver side”phenomenon, exist-
ing as a “template”in the nervous system of the
receiver. Even if all receivers perceived the world in the
same way, they could each still learn different subsets
of molecules from the chemical profile as the signature
mixture of an individual. A further complication
comes from the way that each receiver smells a slightly
different world, because one of the characteristics of
olfaction is the variability of olfactory receptors
between individuals –each of us smells a different
world (Box 1.1) (Chapters 9 and 13). For this reason
too, the learned signature mixtures could differ
between receivers.
With perfect knowledge, one could know the whole
chemical profile of an animal, which molecules from
this profile are learned as the signature mixture by the
receiver, and how the signature mixture is represented
as a template in the nervous system of the receiver. An
outline of what can already be achieved, treating the
system as a “black box,”is shown by experiments with
the ant Formica japonica, which showed that the
nestmate “label”could be reproduced with synthetic
hydrocarbons matching the colony cuticular hydro-
carbons (CHCs) (Akino et al. 2004).
1.1.3 Which sensory systems, olfaction or
gustation, are used to detect pheromones and
signature mixtures?
In both invertebrates and vertebrates, gustatory (taste)
receptors come from different families of receptors
from olfactory receptors, and link to the brain in dif-
ferent, simpler, ways from the olfactory pathways (in
mammals olfaction includes both the main olfactory
system and vomeronasal organ-accessory olfactory
system; see Chapter 9 for more explanation). Most
pheromones seem to be processed by olfaction.
However, a small but significant proportion of pher-
omones in invertebrates are processed by taste (gus-
tation) (Chapter 9). These include the response of a
male Drosophila melanogaster’s gustatory receptors
on its front leg to CHC pheromones important in sex
and species recognition (Chapters 3 and 9). Some
allohormone pheromones in both vertebrates and
invertebrates may act directly on the brain or other
organs (see Section 1.11).
Table 1.1 (cont.)
Pheromone Signature mixture
Processing Mostly combinatorial across glomeruli. Combinatorial across glomeruli.
Detection system:
olfaction or taste
or act directly.
Mostly by glomerularly organized olfac-
tory system(s).
A minority of pheromones by other
chemosensory routes e.g., taste (gestation).
Allohormone pheromones act directly on
tissues or nervous system.
Glomerular olfactory system(s).
In vertebrates with
a vomeronasal
system (VNS).
Detection by the VNS or main olfactory
system or both, depending on pheromone
and species.
Detection by the VNS or main olfactory
system or both, depending on species.
1.1 Intra-specific semiochemicals
|
15
All signature mixtures are likely to be processed by
the combinatorial processes of olfaction rather than
taste (gustation), in part because discrimination
learning is likely to be involved (see Box 9.1).
1.2 “Innateness”of pheromones
Generally speaking, pheromones do not require
learning: they seem to be “innate,”“hardwired,”pre-
disposed, or “work out of the box”(Table 1.2).
However, being innate is not part of the original
pheromone definition (Karlson & Lüscher 1959) or its
updated version (Box 1.2) (see also Sections 1.8 and
9.6) (Wyatt 2010). Instead, the defining point for
pheromones is that they are species-wide rather than
that they are innate (for example, it would be possible
for a pheromone to rely on early learning so long as
typically all individuals imprint on the same molecule
(s) in normal circumstances).
The idea of “innate”behavior is itself a long-debated
question in animal behavior. Seemingly innate
behaviors often have developmental and environ-
mental requirements for full expression (Bateson &
Mameli 2007; Mameli & Bateson 2011). Part of the
problem is that the term “innate”covers many differ-
ent phenomena (Mameli & Bateson 2011). In practice,
trying to separate the contributions of nature (genes)
and nurture (environment) to the development of a
behavior is like asking whether the area of a rectangle
is due more to its length or width (ascribed to psy-
chologist Donald Hebb, in Meaney 2001).
Gene–environment interactions on behavior are
explored by Bendesky and Bargmann (2011).
Just as a mammal’s visual cortex does not form
correctly if the eyes do not receive visual stimuli
during critical periods after birth (Hensch 2004),
olfactory stimuli in amniotic fluid before birth can
influence olfactory bulb development (e.g., Todrank
et al. 2011). Normal responses to pheromones may
not develop unless species-specific conditions are
met. These usually occur as a matter of course in
normal development. Experiments that “dissect”the
developmental process can expose the normally hid-
den mechanism(s) by which a response develops. For
example, perhaps surprisingly, early imprinting on
species-specific odors can be important in recogni-
tion of a mate of the correct species when adult
(Chapters 3 and 9) (Doty 2010, p. 39 ff.; Owens et al.
1999). Normally, as the parents are of its own species,
this leads to appropriate courtship choices, but cross-
fostering experiments can demonstrate that these
olfactory choices are learned in some species such as
pygmy mice, house mice, sheep, and deer (Doty 2010,
p. 39 ff.). Cross-fostered young are attracted to the
species of their foster parents.
In the wild, this learning can be important in
sexual selection and speciation in some species
(Verzijden et al. 2012). Cross fostering showed that
early olfactory imprinting by young fish (learning at
a sensitive period; Chapter 9) normally contributes
to sexual isolation in two stickleback species by
influencing adult mate choices (Kozak et al. 2011).
When adult, learning may also be involved: male
mammals such as rats and mice may need sexual
experience before they can distinguish estrous from
diestrous female odors (Chapter 9) (Swaney &
Keverne 2011).
In some cases, developmental effects have been
shown to act at the periphery of the sensory system: for
example, the behavioral response of young worker
bees to queen mandibular pheromone depends on
exposure to the pheromone soon after pupal emer-
gence, via an effect on dopamine receptor gene
expression in the olfactory sensory neurons (Vergoz
et al. 2009).
Pheromones themselves can prompt learning. While
the response of rabbit pups to the mammary phero-
mone 2-methylbut-2-enal seems hardwired (Box 1.5),
the pheromone stimulates learning of other odors,
which will then also stimulate suckling (Coureaud
et al. 2010; Schaal et al. 2009). Contact with the male
mouse protein pheromone, darcin, prompts a female
mouse to learn both his volatile individual signature
mixture and the location of the scent mark (Chapter 9)
(Roberts et al. 2010, 2012).
16
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Animals in a chemical world
Table 1.2 Biochemical convergence of pheromones among ants, bees, moths and termites, and other animals
including mammals. In some cases, the same or related com pound is used for similar functions in different
species. More commonly, the arbitrary nature of signals is revealed by different uses for same or similar
compound. See other chapters for more details of the functions of these pheromones. After Blum (1982), with
additional information from Kelly (1996), Novotny (2003), Mori (2007) and Breithaupt and Hardege (2012). See
Appendix for notation.
Occurrence
Compound Function Occurrence Animal Genus
Benzaldehyde Trail pheromone
Defense
Male sex
pheromone
Bee, Apidae
Ant, Formicidae
Moth,
Amphipyrinae
Trigona
Veromessor
Pseudaletia
2-Tridecanone Alarm pheromone
Defense
Ant, Formicidae
Termite,
Rhinotermitidae
Acanthomyops
Schedorhinotermes
(R)-(–)-5-Methyl-3-
heptanone;
(S)-(–)-5-Methyl-3-
heptanone
2-heptanone
Female sex pheromone,
male sex pheromone
Male and female
pheromones
Nereid worm
Mammal
Platynereis
Mouse, Mus
Dehydro-exo-
brevicomin
Exo-brevicomin
Male sex
pheromone
Aggregation
pheromone
Mammal
Insect
Mouse, Mus
Bark beetle, Dendroctonus
(Z)-7-Dodecen-1-yl
acetate
Female sex pheromone Mammal
Insect
Female Asian elephant
Elephas maximus & 140 species
of moth (as one component
of a multicomponent
pheromone)
(1S,5R)-(–)-
Frontalin
Aggregation
pheromone
Sex pheromone
Insect
Mammal
Bark beetles
Male Asian elephant E. maximus
(both +/–enantiomers)
1.2 “Innateness”of pheromones
|
17
1.3 How pheromone signals evolve from
chemical cues
The ubiquity and chemical diversity of pheromones
can be explained by natural selection and are the
evolutionary consequences of the powerful and flexi-
ble way the olfactory system is organized (Chapter 9);
gustation (taste) does not have such flexibility. This
may explain why most pheromones are detected by the
olfactory system (in terrestrial vertebrates with both, it
includes the main and accessory olfactory systems).
The olfactory systems of most species have a large
range of relatively non-specific“broadly tuned”
olfactory receptors (Chapter 9). This means that almost
any chemical cue in the rich chemical world of animals
will stimulate some olfactory receptors and can
potentially evolve into a pheromone signal.
Pheromones are evolved signals. Signals alter the
behavior of other organisms, have evolved because of
that effect, and work because the receiver’s response
has also evolved (Maynard Smith & Harper 2003, p. 3;
Seeley 1995, p. 248).
If the signal alters the behavior of the receiver it
must, on average, pay the receiver to respond in this
way, otherwise receivers would evolve not to respond
(Maynard Smith & Harper 2003, p. 3). Signaling is
synonymous with communication as narrowly
defined by Ruxton and Schaefer (2011, p. 2583) in a
helpful discussion of recent debates about animal
communication and information.
In contrast, a cue is any feature of the world, ani-
mate or inanimate, that can be used by an animal as a
guide to future action, but has not evolved for this
purpose (Maynard Smith & Harper 2003, p. 3). For
cues, only the receiver’s response is evolved. For
example, the CO
2
released by an animal as it breathes
can be used as a cue by a blood-sucking insect to find
its host. The mosquito’s response is certainly evolved
(and indeed it has highly specialized receptors to detect
CO
2
), but the release of CO
2
by the host did not evolve
to have the effect of attracting mosquitoes so it does
not count as a signal. The molecules learned in signa-
ture mixtures of kin or familiar animals are probably
best seen as cues rather than signals, as their produc-
tion has usually not evolved for that purpose (see
discussion in Section 1.7).
Scenarios for how chemical cues become phero-
mone signals fall into two main categories: sender pre-
adaptations, with signals starting from chemical cues
released by the sender, and receiver pre-adaptations
selecting for molecules that match the already existing
sensitivity of the receiver (Bradbury & Vehrencamp
2011, p. 377). If the receiver benefits, it may refine its
tuning system. If the sender benefits from the response,
the cue will undergo the evolutionary process of ritu-
alization, becoming a pheromone signal (Bradbury &
Vehrencamp 2011, p. 378; Tinbergen 1952). The
changes in ritualization could include increasing its
conspicuousness (e.g., making it more different from
other similar molecules) and reducing its variability
(stereotypy). Thus pheromones evolve from com-
pounds originally having other uses or significance,
for example from hormones, host plant odors, chem-
icals released on injury, or waste products (Steiger
et al. 2011; Wyatt 2010). There will also be selection
for functional signal features such as longevity and
specificity (Section 1.4). The original functions of the
molecules may or may not be eventually lost.
1.3.1 Pheromone signals derived from
sender precursors
In the sender-precursor model of signal evolution,
pheromones can evolve from any reliable chemical
cue(s) to the sender’s condition (Figure 1.3) (Bradbury &
Vehrencamp 2011, p. 377 ff.). For example, if there are
molecules leaking from a mature female about to lay
eggs, then mutant males better able to detect them will
find her first and gain more matings (Figure 1.3). Over
generations this would result in selection for increas-
ing sensitivity to the female’s molecules (with multiple
copies of such receptors) and changes in the receptors
for greater specificity. The opportunistic co-option of
chemosensory receptor proteins for detection of new
molecules is discussed in Chapter 9. Although a given
odorant may be unlikely to fit any one receptor
18
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Animals in a chemical world
perfectly, it is likely to stimulate some. In turn, if the
sender benefits, in the fish example the female would
benefit by attracting males to fertilize her eggs, then
production and release of the molecules can evolve
into a signal (pheromone). Molecules become a pher-
omone only if there is positive selection on both sig-
naler and receiver.
Such a scenario has been suggested to explain the
use of body-fluid molecules as pheromones by marine
polychaete worms, released with their gametes, which
immediately prompt the other sex to release its game-
tes (Chapter 3) (Figure 3.2) (Breithaupt & Hardege
2012). Similarly, hormones have been co-opted as sex
pheromones in fish, excreted in urine or across per-
meable membranes such as gills (Figure 1.4) (Chung-
Davidson et al. 2011; Stacey & Sorensen 2011). Species
specificity of these multicomponent fish sex phero-
mones comes from other molecules (Section 1.4)
(Levesque et al. 2011; Lim & Sorensen 2012). In ter-
restrial animals such as elephants and mice, many
pheromones are excreted in the urine and though not
necessarily hormones themselves, the quantities and
qualities reflect hormonal levels related to body con-
dition (Section 1.6.2).
The aggregation pheromones used by bark beetles
may have evolved from the molecules produced by the
Ancestral
Spying (Change in receiver)
Communication (originator becomes signaler)
No specialized mechanisms for
detection or response
Evolution of detection and response
Receiver benefits
Receiver's response selects
for signal specialization
CHEMICAL
CUE
SIGNAL
Chemical released
to the water
Chemical and its
release unchanged
Changes in chemical
and/or its release
Response
Receiver
Originator
Receiver
Originator
Receiver
Signaler
X
Figure 1.3 The sender-precursor model of
signal evolution. Proposed stages in the
evolution of a communication function for
molecules released by an “originator”ani-
mal (the potential sender). The × in the upper
panel indicates that the receiving individual
has no special adaptations to receive the cue
beyond detecting it. The process starts with
an association between a cue and a condi-
tion of the originator. Receivers must be
able to perceive or evolve receptors for the
cue, and then incorporate the information
into a decision rule and a response. In this
“spying phase”only the receiver benefits.
The transition to bilateral benefit to both
sender and receiver could occur later if there
is a selective advantage to the sender, lead-
ing to ritualization of the signal to maximize
information transfer.
An original figure by Ivan Hinojosa
(www.flickr.com/photos/ivan_hinojosa) in
Wyatt (2011), inspired by, and with text
adapted from, Stacey and Sorensen (2006)
(with permission from the authors).
Additional text adapted from Bradbury and
Vehrencamp (2011, p. 377).
1.3 How pheromone signals evolve from chemical cues
|
19
beetles’detoxification of the toxic monoterpenes used
by the host trees as a defense against beetle attack
(Chapter 4) (Blomquist et al. 2010). Some of the
detoxification enzymes may have been co-opted as
biosynthetic enzymes for synthesis of pheromones
by the beetle.
Many alarm pheromones in social insects, which
provoke fight or flight in receivers, appear to have
Figure 1.4 Female hormone pheromones co-ordinate reproduction in the goldfish, Carassius auratus, by primer and releaser
effects on the male (Stacey & Sorensen 2009, 2011). It is likely that the hormones evolved into pheromones following the
scenario presented in Figure 1.3.
In the female, the rise and fall of blood concentrations of a succession of hormones (top), from 17β-estradiol (E2) to luteinizing
hormone (LH), steroids, and prostaglandin F
2α
(PGF
2α
), stimulate release to the water of a succession of hormone pheromones
that reflect her hormone levels. First, an unidentified recrudescent pheromone attracts males.
Second, a pre-ovulatory pheromone (the steroid androstenedione (AD), the maturation-inducing steroid 17,20β-P, and its
sulfated metabolite, 17,20β-P-S) are released the night before ovulation. Androstenedione induces agonistic behaviors among
males. As the 17,20β-P:AD ratio increases, males increase their own LH and begin to follow and chase conspecifics. Males
exposed to the pre-ovulatory pheromone increase both the quantity and quality of sperm in the milt (semen), increasing the
likelihood of reproductive success.
Third, post-ovulatory pheromone (prostaglandin F
2α
(PGF
2α
)) and its major metabolite 15K-PGF
2α
stimulate both male
courtship and spawning behaviors and additional male LH increase.
All hormonal cues are released in quantities that range from 10 to >100 ng/h, are detected at concentrations in the picomolar
range, and act in concert to synchronize male behavior and physiology with the female. Figure from and caption after Stacey
and Sorensen (2009).
20
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Animals in a chemical world
evolved from defensive compounds released by fight-
ing or injured conspecifics (Chapter 8). There will be a
selective advantage to the potential receivers sensitive
to these compounds and responding appropriately to
protect the colony. Over evolutionary time, defensive
compounds may gain a signal function: for example,
many ant species use the same chemicals for defense
and alarm, to repel enemies and to alert and recruit
nestmates (Hölldobler & Wilson 1990, p. 260). One
example is the use of volatile formic acid for both
functions in Formica ant species (Blum 1996).
1.3.2 Pheromone signals derived from receiver
sensory bias
Any secreted molecule from a sender that overlaps the
receiver’s pre-existing sensory sensitivities, such as for
food odors, is likely to be selected over others and thus
potentially become a signal (Figure 1.5) (Arnqvist
2006; Bradbury & Vehrencamp 2011, p. 391 ff.;
Endler & Basolo 1998; Ryan 1998). For example, as
female moths use plant odors to find host plants when
egg laying, their olfactory system is already tuned to
these odors: male moth pheromones appear to have
evolved to exploit this female sensory bias (Chapter 3)
(Figure 1.5) (Birch et al. 1990; Phelan 1997). The male
sex pheromone of the European beewolf, Philanthus
triangulum,(Z)-11-eicosen-1-ol, may exploit a pre-
existing female sensory bias for this molecule as it is a
characteristic volatile molecule given off by its hon-
eybee prey (Chapter 3) (Kroiss et al. 2010; Steiger et al.
2011). In Iberian rock lizards Iberolacerta cyreni (for-
merly Lacerta monticola), a pre-existing sensory bias
in females for a food chemical found in their insect
prey, the lipid cholesta-5,7-dien-3-ol (provitamin D
3
),
may have driven selection of this molecule as a com-
ponent of the pheromone secreted by males in their
femoral glands (Martín & López 2008, 2010a) (though
see Font et al. 2012). It is possible that this is also an
honest signal (index) that only high-quality males can
display (Section 1.6.2.1).
As well as the adaptive sensory biases above, there
could also be hidden preferences (“receiver
psychology”), which are incidental side effects of how
the sensory system is constructed (Arak & Enquist
1993; Arnqvist 2006; Bradbury & Vehrencamp 2011,
p. 391 ff.; Guilford & Dawkins 1991, 1993). Such side
effects include what a receiver finds easy to detect,
easy to discriminate, and easy to learn. I wonder if an
animal’s range of olfactory receptors and olfactory
“brain circuits”might lead to such effects.
Many sex pheromones that initially evolved by
exploiting sensory biases may benefit the receiver, by
speeding finding of a mate for example, and rituali-
zation will refine the signal and tune its reception (3b
in Figure 1.5) (Bradbury & Vehrencamp 2011). In other
cases, where there are costs to the receiver in
responding, there may be sexually antagonistic
co-evolution in the subsequent evolutionary elabora-
tion of sexual traits, as the receiver is selected to evade
the “sensory trap”(Arnqvist 2006). In internally fertil-
izing species, one example may be the molecules that
males pass to the female along with sperm (Chapters 3
and 9) (Arnqvist & Rowe 2005; Eberhard 2009;
Poiani 2006). The sex peptides in the seminal fluid of
Drosophila interact with the internal receptors the female
uses to regulate reproductive rate and delay remating,
at a potential cost to herself and a benefitinpaternity
to the male (Section 1.11). The great variety of sex
peptides may reflect the continuing sexually antagonis-
tic co-evolution between male and female Drosophila.
1.3.3 How do we know that a chemical signal has
“evolved for that effect”in the sender?
The definition of a signal includes a requirement that
the signal should have evolved in the sender for the
effect it has on the receiver (above). In some cases we
can identify evolved structures that produce the signal.
For example, in moth females we can see the specialized
pheromone glands evolved for secreting and releasing
the female sex pheromones (Cardé & Haynes 2004;
Liénard et al. 2010). The specific enzyme pathways for
producing the pheromones are also well understood
(Chapter 3). In other animals, we may not know the
source of the pheromones other than a likely tissue, as
1.3 How pheromone signals evolve from chemical cues
|
21
for example the male sex pheromone 3-keto petromy-
zonol sulphate of the sea lamprey, Petromyzon marinus,
is produced in the liver and then released from speci-
alized gland cells in the gills (Siefkes et al. 2003).
In other cases, the response to a cue is adaptive but it
is not clear a signal has evolved. For example, male
Drosophila melanogaster stop courting a female if they
detect the cis-vaccenyl acetate left by an earlier mat-
ing male (Chapters 3 and 9). Similarly, red-sided garter
snake males stop courtship if they detect volatiles from
the ejaculate of a previous male (Chapter 3) (Shine &
Mason 2012). In both species, this is an adaptive
Food detector
(a)
Latent biasesAdaptive sensory biases
1. Sensory bias
and associated
response
Predator detector
Navigation mechanism
Neural wiring
Receiver
psychology
2. Sender benefits
by evolving
matching trait
Ritualization
–+
Tuning
ver
ance
Decouple bias
and response
Receiv
resista
3b. Receiver
benefits
3a. Negative effect on
receiver fitness
4. Improved discrimination, shift
in sender trait or adaptive bias
Figure 1.5 Signals that exploit the
existing senses of the receiver will be
selected for.
(a) Receiver–precursor model of sig-
nal evolution. Shaded boxes represent
receiver steps, white boxes sender steps;
dashed gray arrows (
-----
)indicate
positive fitness effects, dotted black
arrows (
-----
)indicatenegativeeffects.
The first step (1) is the evolution of a
sensory bias and coupled response in a
non-communication context, such as
food detection. Senders evolve a trait
that matches or stimulates the sensory
bias and exploit the associated response
(Step 2). If the receiver benefits (Step
3b), then it may fine tune its sensory
system, and the sender’straitmaybe
ritualized to match the bias better. If the
receiver experiences costs (Step 3a), it
will attempt to resist exploitation by
changing its sensory bias, which may be
costly, and the sender may counter this
move, initiating a cycle of antagonistic
co-evolution. If the receiver can escape
from the sensory trap (Step 4), the bias
and the response will become
decoupled. Figure and caption after
Bradbury and Vehrencamp (2011).
(b) A male oriental fruit moth,
Grapholita molesta, displays its hair
pencils in courtship to a female. The
male’s hair pencils are loaded with
plant-derived pheromones including
ethyl trans-cinnamate (inset), a signal
that may have evolved through sensory
drive exploiting female sensitivity for
odors present in their fruit food
(Löfstedt et al. 1989). The females pre-
fer males with the most cinnamate.
Photograph by Tom Baker.
OCH2CH3
O
(b)
22
|
Animals in a chemical world
response from the other males as a female will not
mate again for some days, given the effects of the sex
peptides in the female Drosophila (Section 1.11) and
with the copulatory plug in place in the case of the
female snake. The male molecules prompting the
response would certainly be cues. Whether or not you
call these molecules pheromones will depend on
whether the first male’s molecules have evolved for
this function.
All biological systems are evolving, so for a given
species we may be at any point on the continuum from
cue to signal. As when defining species in the process
of diverging, we are “dichotomizing a continuum.”In
practice it may be difficult to establish that production
and emission have both evolved, so I propose an
operational definition for pheromones (see Box 1.4).
However, for molecules to be treated as a signal under
the “operational definition,”there also needs to be a
credible evolutionary pathway by direct or kin selec-
tion. For example, fish have evolved sensitive
responses to molecules released when other fish are
injured by predators. However, these molecules are
probably alarm cues rather than an evolved signal as
the responding fish are unlikely to be kin and may
even be from a different species (Chapter 8) (Ferrari
et al. 2010; Wisenden 2014).
1.3.4 Pheromone characteristics, transmission
medium, and signal duration
Whether pheromones evolve from sender precursors or
are derived from receiver sensory bias, which mole-
cules become pheromones is also a product of the
function of the message, as well as the medium the
message will be carried in. For example, in air, ant
alarm pheromones are volatile, with low molecular
weights of between 100 and 200, diffusing rapidly and
dropping below threshold quickly once the danger has
passed (Chapters 8 and 10) (Hölldobler & Wilson 1990).
In water, solubility of molecules is perhaps the func-
tional equivalent of volatility in air. Aquatic phero-
mones range from small molecules such as the amino
acid L-kynurenine used by masu salmon,
Oncorhynchus masou, as a female sex pheromone
(Yambe et al. 2006) to polypeptides and proteins,
which, despite their large size, can be highly soluble,
such as those used as sex pheromones (attractin, enti-
cin, seductin, and temptin) by the marine mollusc
Aplysia (Cummins & Degnan 2010; Cummins et al.
2007).
Volatility or solubility is less important if phero-
mones are transferred directly from signaler to
receiver: male Danaus gilippus butterflies drop crys-
tals of the pheromone danaidone from their hair pen-
cils directly onto the antennae of the female
(Eisner & Meinwald 1995, 2003). The male of the
terrestrial salamander, Plethodon shermani, directly
transfers his high molecular weight glycopeptide
pheromone from his chin gland to the nostrils of the
female (Section 1.4.3.3) (Houck 2009; Woodley 2010).
Different durations of signal life can evolve.
Whereas sound and visual signals only act at the time
they are made, chemical messages can “shout”long
after the signaler has left. Selection can act on the
chemical characteristics of pheromones such as vola-
tility and stability, giving signal durations from the
seconds of ant alarm pheromones (above) (Chapter 8)
to the months or years of some termite trail phero-
mones (Chapter 7) (Bordereau & Pasteels 2011). The
molecules that add longevity to signals have been
identified in some species. Dominant male rabbits,
Oryctolagus cuniculus, secrete a molecule,
2-phenoxyethanol, in their chin secretion used to mark
their territories (Hayes et al. 2003). The molecule does
not seem to be part of the signal but it is used in the
perfume industry as a fixative and seems to have the
effect in tests of extending the life of volatile com-
pounds in scent marks. In the male secretion of
Heliconius melpomene butterflies a similar role is
proposed for fatty acid esters that slow the evaporation
of the volatile male anti-aphrodisiac pheromone,
which includes (E)-β-ocimene (Chapter 3) (Schulz et al.
2008). Similarly, major urinary proteins in mouse
urine slowly release bound volatiles, prolonging the
life of signaling volatiles in scent marks from minutes
to more than 24 hours (Hurst & Beynon 2004).
1.3 How pheromone signals evolve from chemical cues
|
23
1.4 Pheromone diversity, specificity,
and speciation
Pheromones are well known for their species specific-
ity, with animals only responding to the pheromones
of their own species. If there is such specificity, how do
pheromones change as species diverge? This is
explored in Section 1.4.3. First, I cover cases where
pheromones are shared –in both related and unrelated
species –and cases of multiple messages from one
pheromone, before discussing the ways in which spe-
cies can have unique pheromones. The broad-brush
diversity of pheromone molecules comes from the
processes of evolving from chemical cues, as molecules
of all kinds are co-opted as signals (Section 1.3). A
finer grain of diversity comes from the variations
around a “chemical theme”as part of speciation.
1.4.1 When the same molecules are used as
pheromones by different species or taxa
Species may share pheromone molecules if there is no
evolutionary selection for species specificity. For
example, there is usually little need for privacy in
communication for alarm pheromones, and in ants
these are often shared by related species (Chapter 8).
Similarly, the alarm pheromone (E)-β-farnesene is
shared by aphid species across more than 30 genera
(Byers 2005) whereas aphid sex pheromones are
species-specific multicomponent blends (Dewhirst
et al. 2010). Oviposition pheromones in Culex mos-
quitoes, which lead other females to lay near previ-
ously laid egg masses, seem to show cross-species
attraction, perhaps because the benefits of predator
dilution are not species specific (Chapter 4)
(Seenivasagan & Vijayaraghavan 2010). Larval lamp-
reys of different species appear to release a common
pheromone, petromyzonol sulfate and allocholic acid,
to which adults of other lamprey species are attracted
(Chapter 12) (Fine et al. 2004). Moth species that live in
different places may share a pheromone blend as they
will not meet. If moth species live in sympatry (in the
same geographic area) they can have the same
pheromone blend so long as they use different calling
times or host plants to avoid cross-attraction
(Chapter 3) (Cardé & Haynes 2004).
A different phenomenon occurs with pheromones
shared not because of near-relatedness but by con-
vergence. Across the animal kingdom, species that are
not closely related may share the use of a molecule as a
signal, illustrating the independent evolution of par-
ticular molecules as signals (Table 1.2) (Kelly 1996;
Novotny 2003); for example, variations of the terpene
brevicomin are used by male house mice and some
bark beetle species (Novotny, 2003). The Asian ele-
phant female pheromone, (Z)-7-dodecen-1-yl acetate
is a component of the female pheromone blend of
some 140 species of moth, and the Asian male ele-
phant’s pheromone frontalin is also used by some bark
beetles (Rasmussen et al. 1997, 2003). The use of the
same molecules may reflect some constraints on the
number of low molecular weight molecules that are
volatile, stable, and relatively non-toxic. Such coinci-
dences are also a consequence of the common origin of
life: basic enzyme pathways are common to all multi-
cellular organisms and most classes of molecule are
found throughout the animal kingdom.
1.4.2 Different messages from the same
pheromone molecules
Pheromonal parsimony, a species taking different
meanings from the same molecule at different con-
centrations and/or different social contexts, is found
in many animals and is common in social insects
(Blum 1996; Bordereau & Pasteels 2011; Hölldobler &
Wilson 2009, p. 179). Perhaps, once an animal has the
receptors and neural circuitry for a specific phero-
mone, these can be co-opted by other communication
needs. For example, in a number of termite species
such as Pseudacanthotermes spiniger, the same mole-
cule is used at low concentrations as a trail-following
pheromone by foragers and by sexual males during
tandem running (Bordereau & Pasteels 2011). When
released at higher concentrations by female repro-
ductives, it attracts males from long distances and
24
|
Animals in a chemical world
elicits typical sexual excitement behaviors when males
contact it.
The phenomenon is also well illustrated by the
mandibular pheromone of queen honeybees, which is a
sex pheromone for males (drones) and, with additional
pheromone components, has a releaser effect in
attracting workers as the retinue pheromone and also
has primer effects suppressing worker reproduction
(Chapters 6 and 9) (Section 1.9) (Grozinger 2013;
Kocher & Grozinger 2011; Slessor et al. 2005). The
primer and releaser effects may act via different
receptors and nerve circuits (Kocher & Grozinger
2011). In the nematode Caenorhabditis elegans, over-
lapping sets of ascaroside molecules are the sex pher-
omone active at picomolar concentrations and, at
about 10,000 times higher concentrations, the dauer
pheromone, which induces a resistant resting stage in
larvae (Figure 1.6) (Pungaliya et al. 2009; Srinivasan
et al. 2008, 2012).
Pheromonal parsimony also occurs in mammals.
The same molecules, such as male mouse pheromones,
can have different effects on other males and on
females (see Chapter 9). Rabbit mammary pheromone
(Box 1.5) elicits suckling responses from pups and also
stimulates learning of any co-occurring odorant such
as the mother’s odors (Coureaud et al. 2010).
1.4.3 Specificity and the evolution of pheromones
There are two main ways of gaining specificity in
pheromone signals, making a unique signal. One, less
common, way is to use a single unusual molecule (see
below). The alternative, found in most species across
the animal kingdom, is to use a multicomponent
pheromone: a particular combination of molecules,
which individually may not be unusual and may
overlap with those used by related species. The com-
bination makes the pheromone unique.
In most biological signaling systems, sexual selec-
tion (Chapter 3) leads to species-specific sex phero-
mones and responses, important for pre-mating
isolation and speciation in both vertebrates and
invertebrates (Smadja & Butlin 2009). Chemical
communication achieves specificity in different ways
from visual and acoustic communication, which are
continuous spectra, varying in wavelength and tem-
poral structure. By contrast, molecules can differ in
many dimensions including stereochemistry.
Stereoisomers are molecules that have the same
atoms connected in the same order but differ in the
arrangement of atoms in space, changing the shape of
the molecule (Appendix). For both a chemosensory
receptor detecting a molecule, and the enzymes syn-
thesizing it, a molecule’s shape is a key part of inter-
acting with it (Chapter 9) (Reisert & Restrepo 2009).
As a result, stereoisomers are usually treated by
receptors as different molecules (so proper chemical
identification of pheromone molecules must include
stereochemistry). Some stereoisomers are enantiomers,
mirror images of each other (said to be chiral, from
the Greek meaning hand) (Mori 2007). Some pairs of
species gain specificity by using different enantiomers
of the same compound; for example, among sympatric
scarab beetles in Japan, the Japanese beetle, Popilla
japonica, uses (S)-japonilure as its female sex phero-
mone whereas the Osaka beetle, Anomala osakana,
uses (R)-japonilure (see Appendix for notation)
(Leal 1999).
1.4.3.1 Single unique molecule pheromones
A few species have a pheromone consisting of a single
unusual molecule: for example, the female sex pher-
omone of the brown-banded cockroach, Supella
longipalpa, is the single unique molecule supellapyr-
one (Gemeno et al. 2003). Most other cockroach spe-
cies use multicomponent pheromones (Gemeno &
Schal 2004) (see below). Animals using peptide pher-
omones can evolve peptides with amino acids in
unique combinations and sequences. For example,
the decapeptide pheromones of the related species of
Japanese newt, Cynops ensicauda and C.pyrrhogaster,
differ by just two amino acids (Chapter 3) (Toyoda et al.
2004). There are some single small-molecule mammal
pheromones such as the rabbit mammary pheromone,
2-methylbut-2-enal (Box 1.5) (Schaal et al. 2003).
1.4 Pheromone diversity, specificity, and speciation
|
25
OH
O
E. coli OP50 lawn
5 mm
Scoring regions
control
sample
**
**
80
100
120
140
160
0
20
40
60
Mean time i
n scoring region [s]
Mean time in scoring regi on [s]
control
sample
***
150
200
250
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50
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***
ascr#2
ascr#3
ascr#8
asccr#3/ascr#8
ascr#2/ascr#6
ascr#2/ascr#3
N2
daf-22
daf-22/ascr#2/#3
daf-22/ascr#2/#3/#8
ascr#2/#3/#8
O
O
O
OH
O
OH
HN
O
Aggregation
(fM-pM)
Male Attraction
(pM-nM)
Dauer Formation
(nM-µM)
O
H
3
C
HO
O
OH
O
O
H
3
C
HO
O
OH
OH
O
O
H
3
C
HO
O
OH
OH
O
ascr#2
ascr#3
ascr#5
ascr#8
icas#9
O
H
3
C
H
3
C
HO
O
OH
O
H
N
CO
2
H
icas#3
O
H
3
C
O
OOH
O
HN
(b)
Terminus
Lipid side
chain
ascarylose
Head group
O
H
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C
O
O
OH
O
H
N
CO
2
H
HN
O
(a)
(d)
(c)
(f)
(e)
26
|
Animals in a chemical world
However, I think it is likely that when more mamma-
lian sex pheromones are identified it may emerge that,
if they are not peptides, many gain species specificity
by being multicomponent (next section).
1.4.3.2 Multicomponent pheromones
Most pheromone specificity is achieved by using a
combination of compounds as a multicomponent
pheromone that only works as a whole (synergy, see
below). (These are not the same as signature mixtures;
Table 1.1.) The molecules of a multicomponent pher-
omone need not be unusual themselves. It is the par-
ticular combination that gives specificity. For
example, female sex pheromones in moths usually
consist of multicomponent blends of five to six
hydrocarbons (10 to 18 carbons long) including
unbranched fatty acids, alcohols, acetates, or alde-
hydes in particular combinations and ratios (Chapter 3)
(Cardé & Haynes 2004; de Bruyne & Baker 2008).
Because of the way that odor signals are carried in the
wind, all the molecules travel together, so the whole
multicomponent blend is perceived by a responding
male, even far downwind (Chapters 3 and 10) (Linn &
Roelofs 1989; Linn et al. 1987).
Vertebrate pheromones may be multicomponent
too. Two compounds isolated from the urine of male
mice, Mus musculus, provoke aggressive behavior in
conspecific males: dehydro-exo-brevicomin and 2-
sec-butyl-4,5-dihydrothiazole (Chapter 9) (Novotny
2003; Novotny et al. 1999b). For this effect, both
compounds have to be present together and in addition
they need to be presented in mouse urine. The closely
related species of goldfish, Carassius auratus, and
carp, Cyprinus carpio, share a set of five hormonal
compounds that mediate pre-spawning hormonal
surges and reproductive behavior (Figure 1.4)
(Stacey & Sorensen 2009), but these form species-
specific multicomponent pheromones with other mol-
ecules, as yet unidentified, so cross-attraction does not
occur (Levesque et al. 2011; Lim & Sorensen 2012).
Nematode worms from several different clades
(branches) produce species-specific but partially
overlapping mixtures of ascarosides, a family of mol-
ecules unique to nematodes (Figure 1.6) (Choe et al.
2012). These multicomponent pheromones mediate a
variety of nematode behaviors including avoidance,
sex, developmental diapause, and long-range attrac-
tion. Social insect pheromones of many kinds are
multicomponent and the components for a pheromone
Figure 1.6 Multicomponent pheromones and synergy. Sex, aggregation, and dauer (resting stage) pheromones in the
nematode Caenorhabditis elegans are made up of overlapping combinations of related molecules whose action also depends on
concentration (a, b). Synergistic blends of non-indole ascarosides induce dauer at nanomolar to micromolar concentrations and
function as a male attractant at picomolar to nanomolar concentrations, whereas indole ascarosides icas#3 and icas#9 act as
hermaphrodite attractants and aggregation signals at femtomolar to picomolar concentrations (Srinivasan et al. 2012). (c) C.
elegans on a gel in a bioassay (Srinivasan et al. 2012). Each worm is about 1 mm long.
Synergy: individual components of the sex pheromone are no more attractive to males than the control (e) when presented
singly in the bioassay (d), crosses mark the starting positions of assayed animals (Pungaliya et al. 2009). However, when
particular combinations of two ascarosides (ascr#2 and ascr#3) and (ascr#2 and ascr#8) are presented together, a strong
attraction is observed, right columns in (e). This effect is synergy: the components together are the message. In (e) ascr#2 and
ascr#8 were tested at 100 fmol and ascr#3 at 10 fmol. At these concentrations, ascr#3 and ascr#8 did not show a strong synergy.
(f) Wild-type (N2) C. elegans metabolite extract has strong male-attracting activity, whereas mutant daf-22 metabolite extract
is inactive. A mixture of ascr#2 and ascr#3 in amounts corresponding to those present in the wild-type metabolite extract (20
fmol each) added to the inactive daf-22 metabolite extract partially restores activity but full male attraction is restored by adding
ascr#2, ascr#3, and ascr#8 (20 fmol of each). Adding daf-22 metabolite extract does not further increase activity.
See Chapter 2 for the way ascr#2 and ascr#3 were identified by activity-guided fractionation, and how ascr#8 and the indole
ascarosides were discovered by a different technique (Pungaliya et al. 2009; Srinivasan et al. 2008, 2012). Another naming
convention uses “C1”etc., for these molecules, see Edison (2009) for a key.
1.4 Pheromone diversity, specificity, and speciation
|
27
can come from different glandular sources and differ-
ent families of molecules, by different enzyme path-
ways (see Chapters 6, 7, 8, 9, and 10). The ant trail
pheromone in one species, Leptogenys peuqueti, con-
sists of a blend of as many as 14 compounds (Morgan
2009). Social insects may use components in slightly
different combinations for co-ordination of colony
dynamics (Chapters 6 and 9) (Section 1.4.2) (Le Conte &
Hefetz 2008; Slessor et al. 2005).
The prevalence of multicomponent pheromones
may reflect how pheromone signals diverge in speci-
ation (Chapter 3). Within closely related taxonomic
groups of moths (families or subfamilies), species often
use combinations of the same or similar components,
as a result of sharing biosynthetic pathways by
ancestry (Cardé & Haynes 2004; de Bruyne & Baker
2008; Symonds & Elgar 2008). Even where unusual
molecules are used as pheromones, closely related
species tend to use variations on these, as if exploring
chemical space from a new starting point. In cock-
roaches, each of the long-range sex pheromones
identified to date from different cockroach genera
belongs to a different chemical class, with species in
each genus using different combinations of variations
of the unusual molecule (Eliyahu et al. 2012;
Gemeno & Schal 2004). For example, Periplaneta
species use different combinations of molecules based
on the unusual molecule periplanone. A recent iden-
tification follows the same pattern, with a previously
unidentified natural product and a previously
unknown pheromonal structure for cockroaches found
for the main pheromone component of the cockroach
Parcoblatta lata, a macrocyclic lactone, (4Z,11Z)-
oxacyclotrideca-4,11-dien-2-one (Eliyahu et al. 2012).
This molecule also forms a component of the phero-
mones of related species in the genus.
Synergy: a natural outcome of multicom ponent
pheromones
Synergy describes the phenomenon when any one
component shows little or no activity by itself and only
the complete synthetic mixture has an activity
comparable to the pheromone (Figure 1.6). This is how
multicomponent pheromones are detected. The dis-
covery of nematode sex pheromones is a classic
example. The multiple components of the C. elegans
sex pheromone were revealed during activity-guided
fractionation (Chapter 2), as none of the fractions
showed activity when tested alone, activity came only
when brought together in combination. This indicated
that active components were split between the frac-
tions (Figure 1.6) (Srinivasan et al. 2008).
Synergy is to be expected from multicomponent
pheromones, which gain their specificity by the com-
bination (above). I would suggest that synergy is a
natural outcome of the way multicomponent phero-
mones are processed in the brain. It reflects the com-
binatorial organization of olfaction (see Chapter 9). For
example, in the male moth, the message “fly upwind”
in response to female pheromone is only sent to the
higher brain if all the correct molecules stimulate their
antennal olfactory sensory neurons and the glomeruli
in the brain to which these lead (Chapter 9) (Haupt et al.
2010). The neural circuits can be thought of as acting
like digital logic “AND”gates: if a component is
missing or at the wrong ratio, the stimulus does not go
higher in the brain. Conversely, the circuit gives a
“STOP”if there is activation of olfactory sensory neu-
rons sensitive to a pheromone component of the wrong
species (e.g., Lelito et al. 2008). Nematode multicom-
ponent pheromones are processed by simpler circuits,
without glomeruli, but on these same principles.
1.4.3.3 How does evolutionary change in
pheromones occur?
The details of speciation and pheromone evolution
have been explored in moths, allowing us to dissect the
genetics of both pheromone production and signal
reception (the genes for chemosensory receptors and
neural wiring). We know less about the evolution of
vertebrate pheromones. However, detailed studies of
North American salamanders show rapid and some-
times cyclical changes in their protein courtship
pheromones. In mice the evolution of some of the
28
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Animals in a chemical world
sex-dependent changes in expression of enzymes that
lead to production of a male chemosignal, trimethyl-
amine, has been explored along with its specific
receptor (trace amine-associated receptor 5, TAAR5)
(Li et al. 2013). I will start with moths then turn to the
salamanders (see Chapters 3 and 9 for more details
about moth speciation and also the evolution of pher-
omones in Drosophila species).
Signal divergence with new multicomponent pher-
omone blends in insects (with new ratios or presence or
absence of components) can occur either with changes
in a small number of genes or, in polygenic systems,
changes in many genes (Cardé & Haynes 2004;
Symonds & Elgar 2008). The changes in pheromone
production can involve cis-regulatory DNA sections
controlling gene expression or changes within genes
leading to changes in enzyme binding sites and thus
substrate specificity. Both kinds of changes ultimately
affect which pheromone molecules are produced and
in what ratios and quantities.
A small number of genes affecting substrate spe-
cificities of the pheromone-producing enzymes sepa-
rate two strains of the European corn borer moth,
Ostrinia nubilalis (Chapter 3). Females of the two
strains produce, and respective males respond to, dif-
ferent ratios of the same components of the phero-
mone: the Z-strain uses a 97:3 mix of (Z)-11-
tetradecenyl acetate (11–14:OAc) and (E)-11-
tetradecenyl acetate whereas the E-strain uses a 1:99
mix of Z/E11–14:OAc. The change in blend can be
traced to alleles that give different versions of an
enzyme in the biosynthetic pathway (Chapter 3)
(Lassance 2010; Lassance et al. 2010).
The Asian corn borer moth, Ostrinia furnacalis,
diverged from the common ancestor shared with O.
nubilalis about a million years ago. One suggestion is
that there was a “resurrection”of a long dormant
desaturase gene, for an enzyme that changed the
position of a double bond in the pheromone above
(Roelofs & Rooney 2003; Roelofs et al. 2002). An
alternative possibility is that the desaturase gene was
always active but may have changed from being
expressed in males, as in O. nubilalis, to being
expressed in females in O. furnacalis, changing the
female blend (Chapter 3) (Lassance & Löfstedt 2009).
However, in many moth species, the differences
between multicomponent pheromone blends of
females result from polygenic changes, such as in the
related sympatric species Heliothis virescens and H.
subflexa (Chapter 3) (Groot et al. 2009). In these
Heliothis species, quantitative trait locus (QTL) studies
showed that genes on at least nine of the 31 Heliothis
chromosomes contribute to the pheromone differences
between the species, which may also involve genes
other than those encoding the enzymes themselves.
ThechangeleadingtotheAsiancornborer,O. nubi-
lalis, pheromone has been called a “saltational”shift, and
it has been suggested that “sudden major switches in
pheromone blend and male response appear more likely
than accumulation of small changes”(Roelofs et al.
2002). However, the basis for suggesting a greater like-
lihood of major “saltational”shifts seems to rest on one
simulation model (Butlin & Trickett 1997). While a
comparison of aggregation pheromones in some bark
beetles could fit this idea, the pattern of aggregation
pheromones in Drosophila species appeared to support
gradual shifts (see Symonds & Elgar 2008). My own
feeling is that the general pattern is likely to be gradual
change as evidenced by the radiation of related mole-
cules as pheromones within genera discussed in moths
and cockroaches (Section 1.4.3.2). The polygenic
changes, such as those in Heliothis moths, above, also
suggestthatmodifiers and gradual changes are often at
work (Chapter 3). Dramatic “saltational”changes may be
uncommon. When they occur they are simply part of a
continuum of change, and a largechangeinblendcan
just reflect a genetic change in an enzyme high
“upstream”in the biosynthetic pathway (see Figure 3.15).
When pheromone blends change, will any males
respond to the new pheromone blend? The responses
of males, in moths at least, seem wide enough to cover
some changes (Chapter 3) (Martin et al. 2011a). A
screening of European corn borer, Ostrinia nubilalis,
males in the laboratory showed that some rare, broadly
tuned individuals would fly upwind to the new blend
of the Asian corn borer, O. furnacalis, as well as to the
1.4 Pheromone diversity, specificity, and speciation
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29
blend of their own females (Chapter 3) (Linn et al.
2003; Roelofs et al. 2002). Similar results were found
with some male cabbage looper, Trichoplusia ni,
moths responding to a novel pheromone blend pro-
duced by mutant females (Cardé & Haynes 2004;
Domingue et al. 2009) (Chapter 3). Over the genera-
tions, T. ni males with a greater response to the mutant
blend could be selected for in the laboratory. Changes
can be at the level of olfactory receptor sensitivity but
also in the wiring in the brain. In the European corn
borer moth, Ostrinia nubilalis, the “wiring”of the
pheromone circuits of the brain of males in the two
strains with opposite ratios of Z/E 11–14:OAc is simply
mirrored (Chapter 9) (Karpati et al. 2008, 2010).
Salamanders
The evolution of courtship behavior, morphology, and
male pheromones in North American plethodontid sal-
amanders shows change on long and short time scales
(Figure 1.7) (Houck 2009; Woodley 2010). The male
courtship pheromone, which includes three unrelated
proteins, is produced by his chin (“mental”) gland and
increases the receptivity of the female, shortening
courtship time. Males in most of the 300 or so species
show the ancestral courtship behavior that emerged
about 100 million years ago: they deliver the phero-
mone to the female by depositing the chin secretion on
the female’s back while simultaneously scratching her
skin with enlarged pre-maxillary teeth. The pheromone
passes through the skin into the capillary blood system.
About 19 million years ago, one clade (branch) of sal-
amanders, now represented by about 30 species of
Plethodon, evolved a different delivery route, and the
male instead taps his chin gland directly on the female’s
nostrils, delivering the pheromone to the vomeronasal
olfactory system (VNO) (a “second nose”that many
terrestrial vertebrates have) (Chapter 9) (Figure 1.7).
Along with the change in behavior, the males of these
species also lost their elongated teeth.
The relative stability of courtship behavior over
millions of years on either side of the major changes in
delivery contrasts with the repeated, periodic episodes
of rapid molecular evolution and diversification of the
pheromone in many species, driven by positive selec-
tion acting on one or more of the three proteins of the
19 MYA273542100
+SPF
+ PMF
+ PRF
+ Mental Gland
+ Premaxillary Teeth
– Premaxillary Teeth
+ Transdermal Delivery
+ Olfactory Delivery
P. glutinosus group
Incl udes P. shermani
P. wehrlei group
P. welleri group
P. cinereus group
western Plethodon
Aneides
Desmognathus
Eurycea
D. ocoee
P. shermani
salamandrids
Olfactory
~30 spp
Intermediate
~7 spp
Transdermal
~350 spp
Delivery
Figure 1.7 The evolution of courtship pheromone delivery in plethodontid salamanders in North America. Ancestrally, all the
plethodontid salamanders had the sodefrin-like precursor factor (SPF) protein pheromone and the plethodontid modulating
factor (PMF) protein produced in the mental (chin) gland, protruding pre-maxillary teeth and scratching (transdermal) delivery
of courtship pheromones. Later, in some clades another protein, plethodontid receptivity factor (PRF), and, later still, olfactory
delivery of courtship pheromones and loss of the pre-maxillary teeth evolved. Photographs to the right show olfactory
pheromone delivery by the red-legged salamander, Plethodon shermani, and transdermal delivery by the Ocoee salamander,
Desmognathus ocoee. Photographs Stevan J. Arnold. Figure adapted from Woodley (2010) and data from Kiemnec-Tyburczy
et al. (2011). The cladogram shows the evolution of characters (for more details see Palmer et al. 2007a). The phylogeny at group
level is still in flux, with some phylogenies making the P. wehrlei and P. welleri groups into sister groups.
30
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Animals in a chemical world
pheromone (Figure 1.7) (Houck 2009; Palmer et al.
2010; Woodley 2010). Comparisons of DNA changes
across 27 species for one of the proteins, plethodon
receptivity factor (PRF), showed that some Plethodon
lineages had neutral divergence and purifying selection
with little change over time (Palmer et al. 2005, 2007b).
Other lineages showed rapid, repeated, cyclical evolu-
tion driven by positive selection, probably resulting
from sexual selection leading to co-evolution of the
male pheromone variants with VNO receptors in the
female (it is supposed). Several of the varying codons
appear to be involved in a “molecular tango”in which
the male signal and female receptors co-evolve on a
“dance floor”constrained by the limited number of
allowable amino acid substitutions that still allow the
pheromone protein to interact with the receptor(Palmer
et al. 2005). The same mutations seem to come and go
cyclically, over time. The “molecular tango”is likely
driven by sexual selection, which may be female pref-
erence or, perhaps, sexual conflict as in the fast evolv-
ing sex peptides in Drosophila (Chapter 3)
(Sections 1.3.2, 1.11) (Arnqvist 2006). The other char-
acteristics of the tango include gene duplication,
hyperexpression in the mental (chin) gland, and abun-
dant polymorphism within populations arising from
the tendency to both retain and reinvent sequence
variants (Palmer et al. 2010; Woodley 2010). A similar
and more extreme pattern of change over time and
polymorphism within individual males is shown for a
second protein in the pheromone, plethodontid modu-
lating factor (Palmer et al. 2010; Wilburn et al. 2012).
What we don’t have yet is the receptor side of the story
for any of these pheromone proteins (unlike the moths).
1.5 Production of pheromones
Most pheromones are synthesized and secreted by the
signaler, often from specialized glands (see Section 1.7
for signature mixtures). However, as long as they are a
consistent signal across a species, pheromone mole-
cules or precursors may be collected rather than syn-
thesized from scratch (hence I have changed the verb
in the definition in Box 1.2 to emit rather than secrete).
For example, specialist moth and butterfly species
(Lepidoptera) harvest pyrrolizidine alkaloids (PA) from
plant species containing them (Boppré 1990; Conner
2009). In some specialist lepidopteran species only the
larvae sequester the alkaloids; in others, such as the
milkweed danaine butterflies (Nymphalidae), adults
also feed on these PAs. Courtship in PA-sequestering
species usually involves presentation to the female of
derivatives of these alkaloids. Males without evidence
of chemical gifts are rejected (see Chapter 3)
(Section 1.6.2). Likewise, to display successfully and
attract females, male euglossine orchid bees in the
American tropics must fill specialized hind-leg pockets
with fragrances such as limonene from orchid flowers
and other sources (Ramírez et al. 2011; Zimmermann
et al. 2009). The males get their species-specific pher-
omone mix by collecting from flowers of the correct
orchid species. You could say orchid bees use take-
aways rather than cooking for themselves.
So long as the molecules are consistent across the
species, animals may use molecules produced by bac-
teria as pheromones. Among locust phase change
pheromones are guaiacol (2-methoxyphenol) and
phenol, produced by locust gut bacteria (Box 4.1)
(Pener & Simpson 2009).
The independent and multiple evolution of phero-
mones is illustrated not only by the diversity of mole-
cules used (Section 1.4) but also by the enormous
variety of specialized secretory glands used to produce
them. Among male mammals and male Lepidoptera
(moths and butterflies) the variety is probably largely
the result of sexual selection (Chapter 3) (Andersson
1994; Darwin 1871).
There is an enormous variety of glands and secre-
tions across the social insects (Box 6.1) (Billen 2006).
Genes associated with gland development are among
the most rapidly evolving genes across eusocial bees
and may be related to the convergent evolution of
advanced systems of chemical communication used to
organize eusocial colonies (Chapter 6) (Woodard et al.
2011). The diversity of hundreds of molecules produced
by ants has been termed chemical sorcery for sociality
1.5 Production of pheromones
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31
(Morgan 2008) and it is matched by the diversity of
glands involved: more than 40 anatomically distinct
exocrine glands have been found so far across the ants
(Billen 2006; Hölldobler & Wilson 2009, p.180). The
same gland may produce different molecules in differ-
ent castes of the same species (Box 6.1) (Grozinger
2013; for example the queen and worker honeybees,
Kocher & Grozinger 2011; Le Conte & Hefetz 2008;
Slessor et al. 2005). The components of a social insect
multicomponent pheromone can come from different
glandular sources and different families of molecules,
by different enzyme pathways.
1.6 Pheromones: signal honesty and costs
What is to stop a subordinate male mouse giving off
the pheromones of a dominant male? This is a long-
running question in animal communication: what
keeps signals honest or reliable, so that the receiver can
rely on the signal to reflect the real quality of the
signaler? Generally, it seems that intra-specific signals
are honest
1
(Bradbury & Vehrencamp 2011, p. 397;
Greenfield 2006). What keeps them honest?
In many research papers you will read statements
along the lines of “signals must be costly to make
them honest.”This is not true. It comes from wide-
spread misinterpretations of the literature about
animal communication (Maynard Smith & Harper
2003; Számadó 2011a, b). This is not to say that
signaling cannot be costly –itcanbe,andIgive
some examples below. However, the “must be costly”
statement refers instead to a theoretical idea, the
handicap principle, an idea that is starting to be
questioned again (see Box 1.6). Honest signals do not
necessarily need to be costly. Showing that a signal
has a cost does NOT demonstrate a handicap
(Számadó 2011a,b).
I need to explain briefly what costs we are talking
about. The straightforward cost of signaling is called
the “efficacy cost,”the minimum cost needed to ensure
the information can be reliably perceived by the
receiver, for example a cricket song loud enough for a
female to hear (Figure 1.8) (Guilford & Dawkins 1991;
Maynard Smith & Harper 1995, 2003). Some signals
are effectively free, with an efficacy cost of almost
zero. The “handicap cost”(also called the “strategic
cost”) is the idea of a specifically wasteful cost on
top of any straightforward efficacy cost of signaling
(Box 1.6) (Figure 1.8).
1.6.1 Efficacy costs of pheromones com pared
with other modalities
How best to measure costs is itself a major question: a
signal could take a lot of energy but have little fitness
Efficacy cost Strategic cost
Production cost
Strategic cost
Efficacy cost
handicaps
minimal-cost signals
cost-free signals
Figure 1.8 Signal types as a function of the cost of producing
them. From the bottom up, signals with almost zero efficacy
cost (the minimum cost needed to ensure the information can
be reliably perceived) are called “cost-free signals.”An
example would be the individual body odor, used by other
animals to recognize an individual. “Minimal-cost signals”
have only efficacy cost. This could be the energetically
expensive secretion of proteins into mouse urine for marking
of territories (but no more expensive, though, than it needs to
be for efficacy). Handicaps have wasteful “added cost”
(“strategic cost”) on top of whatever cost is needed for effi-
cacy (getting the message across). We currently have no
experimental way of separating efficacy and strategic costs
of a given signal and thus no evidence of a strategic cost.
Figure and caption after Számadó (2011b). Terminology from
Guilford and Dawkins (1991); Maynard Smith and Harper
(1995, 2003).
1
Reliable or “honest”signals reveal the relevant quality of
the signaler to the receiver, with the intensity of signal
reliably correlated with the quality (Maynard Smith &
Harper 1995; Számadó 2011a,b).
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Animals in a chemical world
Box 1.6 The problems of signaling costs and the handicap principle
In this box, I explain the more technical background to the conclusions that (1) honest signals do
not necessarily need to be costly and that (2) showing a signal has a cost does not demonstrate a
handicap (Számadó 2011a,b).
Zahavi’s (1975) counter-intuitive “handicap”idea was that signalers, even honest ones, need
to pay an extra wasteful cost, in addition to the efficacy cost (the simple cost of making a signal
that can be perceived by the receiver), to ensure a signal is honest: “waste can make sense,
because by wasting one proves conclusively that one has enough assets to waste and more. The
investment –the waste itself –is just what makes the advertisement reliable”(sic) (Zahavi &
Zahavi 1997, p. 229) (Figure 1.8).
Grafen’s (1990a) models showed, but only for signals between animals that have conflicting
interests, that Zahavi’s ideas could work in a model of evolutionarily stable strategies (ESS): an
additional (strategic) cost for honest signalers at the ESS equilibrium makes their signals reliable
indicators of quality, and it costs a better male less to make the same signal (a differential cost).
Despite the limited scope of Grafen’s model support, restricted to signals between animals with a
conflict of interest (Grafen 1990a, p. 530), Zahavi (2008, p. 2) has claimed “the handicap
principle is an essential component in all signals”(and similarly in Zahavi & Zahavi 1997,
pp. 40, 229–30).
However, there are now many alternative models, of different kinds or using different
assumptions, which show that cost-free or efficacy-cost-only honest signals can evolve without
the need for handicap costs, even for unrelated individuals with conflicting interests. Számadó
(2011a,b) notes these alternative models have variously shown (1) that differential cost criteria
are neither necessary nor a sufficient condition of honest signaling (Getty 2006); (2) that higher
quality signalers need not waste more at the equilibrium than lower quality ones (Getty 2006); (3)
that it is the weak signalers that will use the costlier signal, and not the strong signalers, if there
are no alternatives (Hurd 1997); and that (4) honest equilibrium signals need not be handicaps
(Bergstrom & Lachmann 1998; Bergstrom et al. 2002; Hurd 1995; Lachmann et al. 2001;
Számadó 1999, 2003, 2008).
The assumption that all signals have to be wastefully costly to be honest has dominated
discussion of animal communication and it has in turn skewed the investigation of costs in
pheromones (Section 1.6). Alternative models (above) (reviewed by Számadó 2011a,b), which
support non-handicap solutions tend to be ignored in standard texts on animal communi-
cation (see Further reading). This puts pheromone researchers at a disadvantage as they rely
on these accounts to understand the theoretical basis of communication and how it might
relate to pheromones. Since the challenges to the handicap idea are rarely mentioned, it is no
surprise that individual researchers and reviews of pheromone signals tend to accept the
handicap principle’s ideas without reservations. This has led many researchers, despite the
evidence, to conclude mistakenly that any pheromone costs they find must be “handicaps.”
1.6 Pheromones: signal honesty and costs
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33
cost in evolutionary terms such as survival or future
mating opportunities (Clark 2012; Kotiaho 2001;
Moreno-Rueda 2007). However, given the difficulty of
measuring fitness costs, energy costs are most com-
monly measured.
The size of the efficacy cost, needed simply to con-
vey the information (Figure 1.8) (Guilford & Dawkins
1991; Maynard Smith & Harper 1995, 2003), depends
in large measure on the modality of the signal (whether
it is using sound, light, or chemicals for example).
Creating acoustic signals takes muscular activity and
typically the cost is ~8 times higher than resting met-
abolic rate in ectotherms such as insects and amphib-
ians, and ~2 times higher in birds (Ophir et al. 2010).
Trilling male katydids (Orthoptera) have among the
highest energy consumptions per unit mass of any
acoustic signaler (Stoddard & Salazar 2011). These
high costs are reflected, for example, in male crickets
devoting up to half their daily respiratory budget to
acoustic signaling (Prestwich & Walter 1981).
In contrast, the metabolic cost of most pheromone
signaling is likely to be low compared with that of
other signals, in part because the quantities of
material needed are so small and because, generally,
pheromones are released into the wind or current for
passive transport, not actively pushed by muscle
action to the receiver (Chapter 10). For example, just
40 nanograms of the peptide pheromone of the
magnificent tree frog, Litoria splendida, released
into the water one meter from a female will attract
her to the source in minutes (Wabnitz et al. 1999).
The costs of production are probably similarly low
for many invertebrate pheromones. The lifetime
cost to a male boll weevil beetle, Anthonomus
grandis, to produce its monoterpene sex pheromone
is estimated at only 0.2% of its body weight (Hedin
et al. 1974). Male Caribbean fruit flies, Anastrepha
suspensa, can have their pheromone production
doubled by application of synthetic hormone
(methoprene) (Teal et al. 2000). In laboratory
experiments this doubled their sexual success,
without an increase in mortality (Pereira et al.
2010b). Adding protein to their sucrose diet simi-
larly doubled pheromone production and these
effects were additive, so combined methoprene and
protein supplement produced males four times more
sexually successful than untreated males (Pereira
et al. 2010a) (incidentally this shows the positive
effect of condition on pheromone production). Why
then do males not already double their pheromone
production? The cost of a small quantity of juvenile
hormone (JH) does not seem a likely reason
(Pereira et al. 2010b). Rather, outside the laboratory,
perhaps exaggeration is prevented by the cost
imposed by predators that are attracted by releasing
more pheromone (Section 1.6.2.5).
Nonetheless, pheromone signals can have signifi-
cant efficacy costs. For example, some mammals
Box 1.6 (cont.)
Despite “strategic costs”being a crucial part of the handicap principle, there is currently no
methodology for splitting the costs of a signal into its efficacy costs (just to get the message out)
and strategic ones (the added wasteful costs for a handicap) (Számadó 2011a,b). Indeed the
predictions of the handicap model and index models cannot be separated in many experimental
systems.
The arguments above do not rule out the possibility that the handicap model could apply in
some situations but I think the blanket “signals must be costly to be honest”statement is surely
no longer useful.
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Animals in a chemical world
spend significant amounts of energy on carrier pro-
teins for pheromone signals: in mice, the territorial
male’s urine marks contain 20 to 40 mg ml
–1
of pro-
tein, largely major urinary proteins (MUPs) (Box 5.2)
(Hurst & Beynon 2004). Marking with such large
amounts of protein may have significant metabolic
costs, reflected in lower rates of growth compared with
animals marking less (Gosling et al. 2000). The MUPs
bind the small molecule pheromones, thiazole and
dehydro-exo-brevicomin, slowly releasing them and
thus increasing the attractive volatile lifetime of the
signal from minutes to perhaps 24 hours. One of the
MUPs, darcin, which binds thiazole, is a pheromone in
its own right (Box 1.5) (Chapter 9) (Roberts et al. 2010).
Efficacy costs could also include such things as the
time for a territory owner to revisit and maintain its
scent marks (Chapter 5). Similarly, in species that do
not synthesize their pheromones themselves, efficacy
costs could include the time and energy used to collect
plant materials used as pheromones or pheromone
precursors (Section 1.5).
1.6.2 Reliable signals without handicap
There are many ways for reliable signals to evolve,
without the need for handicaps (Grafen 1990a; LaPorte
2002; Maynard Smith & Harper 1995, 2003; Számadó
2011b). These include index signals (plural: indices),
individual recognition, shared interest, and punish-
ment of cheaters. A given signal could involve more
than one mechanism. None of these mechanisms
require costs beyond the efficacy cost: no wasteful
handicaps are needed.
1.6.2.1 Indices: unfakeable signals
An index signal is one that cannot be faked. Its reli-
ability is maintained by a mechanistic link (physical
connection) between signal intensity and a quality
characteristic of the signaler (Maynard Smith & Harper
1995, 2003). It has an inherent honesty that makes it
unfakeable. For example, male giant pandas,
Ailuropoda melanoleuca, do a handstand to get their
urine marks as high as possible: only a genuinely large
panda can get its mark high on a tree (Nie et al. 2012;
White et al. 2002). Mouse territory scent markings are
an honest index of territory ownership, as only the
owner can exclusively cover the territory with his
urine marks (Chapter 5) (Roberts 2007). A subordinate
male, even if he produced the pheromones of a domi-
nant male, could not hold and mark a territory.
The quantity of pheromone produced by animals
may be an index reflecting quality, leading to “the
success of the smelliest”(Chapter 3) (Wyatt 2009). For
example, female tiger moths, Utetheisa ornatrix,
choose a male with the most pheromone (Chapter 3).
His pheromone is derived from a proportion of the
alkaloid plant poison store that he will pass to the
female at mating, and which she will use to protect the
eggs (Section 1.5). His pheromone load is correlated
with the alkaloid gift he will give (Chapter 3) (Kelly
et al. 2012).
Among fish, male peacock blennies, Salaria pavo,
offer parental care of eggs. The male blennies advertise
with a pheromone produced by the same gland that
produces protective protein secretions for the eggs
(Chapter 3) (Barata et al. 2008a; Serrano et al. 2008).
Bigger glands produce both more pheromone and more
protein secretions (see also below).
Other indices may be related to body condition,
reflecting environmental factors such as nutrition as
well as genetic background (Chapter 3) (Cornwallis &
Uller 2010; Pizzari & Bonduriansky 2010). Links
between condition and quality can simply reflect effi-
cacy costs: handicaps are NOT necessarily required
(Getty 2006; Hill 2011; Maynard Smith & Harper
2003). The links could involve trade-offs of energy
allocation (perhaps mediated by hormones –which
need not be a handicap), or shared pathways for
pheromone production and vital physiological pro-
cesses (Hill 2011). There are many examples of pher-
omones related to condition that influence mate
choice. For example, the attractiveness of a male
Nauphoeta cinerea cockroach is increased with better
1.6 Pheromones: signal honesty and costs
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35
body condition (influenced by greater carbohydrate
intake), because he produces more pheromone (South
et al. 2011). Meadow vole, Microtus pennsylvanicus,
males on a higher protein diet produced more attrac-
tive chemosignals in their urine marks (Ferkin et al.
1997; Hobbs & Ferkin 2011). In rock lizards,
Iberolacerta cyreni, the proportion of oleic acid,
attractive to females, in a male’s scent marks is
dependent on his body condition (Martín & López
2010a,b) (though see Font et al. 2012). Chapter 3 gives
more details of these and other examples.
1.6.2.2 Individual or colony identity
The signals and cues that allow individual or colony
recognition are expected to be cheap and not related to
condition (Tibbetts & Dale 2007). These can be cost free
or minimal-cost signals (Figure 1.8) (Section 1.7). The
molecules may even be cues rather than signals, using
co-opted variation, as in molecules associated with the
MHC. These are likely to be largely cost free. In some
animals, the molecules may be evolved signals pro-
duced for recognition, as may be the case for part of the
chemical profile of CHCs in social insects, which form
the major part of the signature mixtures learned by
nest mates (Section 1.7) but there is no need to assume
a high cost for these (Tibbetts & Dale 2007).
1.6.2.3 Shared interest and relatedness
Signals between animals with a shared interest can be
honest at minimal or no cost (Maynard Smith 1991;
Maynard Smith & Harper 2003). For example, female
moth sex pheromones for long-distance attraction
may be such a signal, as both male and female moths
have a common interest: both gain from meeting to
mate and it does not benefit females to attract any
males apart from ones of their own species. However,
better fed female moths may release more pheromone
(Foster & Johnson 2011), perhaps by an index effect
via hemolymph blood sugar.
Minimal-cost signals are perhaps even more likely
to evolve when the signaler and receiver share a
common interest through being related as kin. The
young of subsocial insects such as burrower bugs,
Sehirus cinctus, release a condition-dependent solic-
itation pheromone when begging for food from their
parents (Kolliker et al. 2006; Mas & Kölliker 2008).
Exaggerated begging by the signaler may be limited
because the extra resources gained by the begging
would be at a cost to its siblings (and hence to its
inclusive fitness) (Moreno-Rueda 2007). Cuckoos are
not restrained in this way as the costs of exaggerated
begging are to the host offspring.
A strong shared interest through relatedness in
social insects such as ants, wasps, bees, and termites
probably makes much of their communication mini-
mal cost (Maynard Smith & Harper 2003). These
include alarm and trail pheromones but also the
queen’s fertility signal pheromone and egg-marking
pheromones (Chapter 6). In the presence of the queen
pheromone, workers’ovaries do not develop and
workers do not lay eggs (Heinze & d’Ettorre 2009; Le
Conte & Hefetz 2008; Peeters & Liebig 2009). This is
likely to be an honest signal rather than “control,”with
the honesty maintained by a combination of related-
ness and worker policing (see Chapter 6 for more details).
Worker policing includes destroying worker-laid eggs,
recognized because they are not tagged with queen egg-
marking pheromone. Workers are selected to respond
to queen egg-marking pheromone in this way as it
allows them to rear more related brothers rather than
the sons of sisters (see next section) (Chapter 6)
(Ratnieks et al. 2006).
1.6.2.4 Punishment of cheaters (social cost)
Honesty can be maintained by punishment of cheating
individuals. For example, in social insects, cheating
workers who develop eggs and thus show the fertility
signal CHCs of a fertile female are punished (see
worker-policing, Chapter 6) (Figure 1.2) (Liebig 2010;
Peeters & Liebig 2009). In bulldog ants, Myrmecia
gulosa, non-laying workers immobilize workers start-
ing to develop their ovaries, revealed by their CHC
profiles (Dietemann et al. 2005). The queen of the ant
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Animals in a chemical world
Aphaenogaster cockerelli herself also detects charac-
teristic fertility signal CHCs on reproducing workers,
and marks them with queen-specific secretion from
her Dufour’s gland, which leads other workers to
attack them (Smith et al. 2012).
Subordinate mice are attacked if they produce the
pheromones characteristic of dominant males and also
if they “challenge”the urine marks of the dominant
male with their own urine (Chapter 5) (Hurst 2009;
Hurst & Beynon 2004).
1.6.2.5 Other costs
Animals may avoid exaggerating their signals not
because of physiological costs but instead because
making oneself more conspicuous brings greater costs
from predation or parasitism (Chapter 11) (Zuk &
Kolluru 1998). For example, the pheromone of
Mediterranean fruit fly males, Ceratitis capitata,
attracts yellowjacket wasps, Vespula germanica,
which eat large numbers of signaling males
(Hendrichs & Hendrichs 1998). This may be what nor-
mally limits pheromone production in males of
another tephritid fruitfly, Anastrepha suspensa, able
to greatly increase their pheromone production in
response to hormone treatment in the laboratory
(Section 1.6.1) (Pereira et al. 2010b).
Exaggerated advertisement of paternal gifts by male
peacock blennies or tiger moths (above), at the expense
of real care or poison-gift protection to offspring, may
have its own costs as a dishonest male would pre-
sumably suffer greater egg losses.
1.7 Chemical profiles from which signature
mixtures are learned for individual and
colony recognition
This section emphasizes learning for kin or group
recognition but the principles apply to other kinds of
learning. How animals distinguish members of their
group from non-members is a key behavior allowing
them to favor offspring and other relatives (kin) or
fellow group members (see reviews by Holmes 2004;
Penn & Frommen 2010; Sherman et al. 1997; Wiley
2013). Kin recognition is also important for optimal
outbreeding by avoiding close kin as mates
(Chapter 3). Recognition of non-kin individuals, such
as mates or neighbors is also important (Wiley 2013).
Odor cue recognition can be used to recognize and
reject previous mates (the Coolidge effect, Chapter 3).
The mechanisms are the same and involve the learning
of cues.
Chemical cues are widely used for recognition, per-
haps because even the earliest organisms had the
receptor mechanisms for receiving and processing the
information and perhaps also because of the enormous
variety of compounds available, which allows an
effectively unlimited number of possible
combinations.
Signature mixtures are the subsets of variable mol-
ecules from the chemical profile (Figure 1.1) that are
learned as a template by other conspecifics and used to
recognize an organism as an individual or as a member
of a particular social group such as a family, clan, or
colony (Chapter 6) (van Zweden & d’Ettorre 2010;
Wyatt 2010). A key difference between pheromones
and signature mixtures is that in all taxa so far inves-
tigated it seems that, with few exceptions, all recog-
nition systems involve learning and all appear to use
the olfactory rather than the gustatory system for
detection (Chapters 6 and 9). Different receivers might
learn different combinations of molecules as the sig-
nature mixture of the same individual (see legend to
Figure 1.1) (Section 1.1.2).
The chemical signature mixtures learned by verte-
brates and invertebrates may be seen best as cues
rather than signals: although the response may be
highly evolved, the signature mixture molecules may
not be evolved specially for this function and may
instead be “co-opted”for this use (Wyatt 2010). For
example, the enormous variability of the major histo-
compatibility complex (MHC) is likely to be driven by
its immune system function (Box 3.1) (Section 1.7.4)
and so the best analogy might be with human finger-
prints, not evolved for the purpose of individual
1.7 Chemical profiles and signature mixtures
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37
recognition but potentially useful for human
identification.
The signature cues learned may simply be mixtures
sufficiently stable and individually different to enable
an animal to recognize the same individual on another
occasion as “familiar”(previously met) or, in some
species, a particular individual (Johnston 2008;
Thom & Hurst 2004; Wiley 2013). Individual recogni-
tion by smell is found in many organisms. Lobsters
recognize each other by smell and avoid fighting a
lobster they previously lost a fight to in the previous
week (Atema & Steinbach 2007). Dominant male mice
mark their territories (Chapter 5). If an experimenter
adds a small urine mark from a resident subordinate,
the dominant male soon attacks that individual (Hurst
1993). In some ant species, unrelated founding queens
use chemical cues to recognize each other individually
(d’Ettorre & Heinze 2005).
In some social insects that use largely hydrocarbon
“labels”under genetic control, colony recognition
blurs the signal–cue boundary (Section 1.3) as these
evolved labels would count as signals (yet the highly
variable labels are characterized by inter-colony var-
iation and changes over time due to other molecules
such as diet, so they do not match the “species-wide”
requirement for a pheromone).
1.7.1 Learning and recognition
Perhaps surprisingly, recognition cues are usually
learned through behavioral “rules,”such as “learn the
odor of your nestmates.”There are three main poten-
tial mechanisms that animals use to recognize others
as kin (Figure 1.9): first, by learning the characteristics
of surrounding individuals (by direct familiarization
with nestmates); second, by using this learning to
allow phenotypic matching with unfamiliar kin; and
third, by using self-inspection –the armpit effect
(Dawkins 1982) –to allow phenotypic matching with
unfamiliar kin. All three mechanisms rely on learning
a memory template. The different mechanisms are not
mutually exclusive and different ones may be used by
the same animal, for example, in different contexts or
at different ages (Mateo 2004; Penn & Frommen 2010).
Self-matching may be favored in species where the
young grow up alone (e.g., crickets, Chapter 3) and
lack contact with kin for learning, or if the avail-
able relatives in the nest would give error-prone tem-
plates, as for example when nestmates include full-
and half-siblings from multiple matings (Mateo 2010;
Sherman et al. 1997). This second situation applies to
the golden hamster, Mesocricetus auratus, which
mates multiply and produces multiply sired litters.
Recognition of kin seems to be by self-referent (“arm-
pit”) matching: hamsters that were reared only with
non-kin since birth responded differently to the odors
of unfamiliar relatives and non-relatives (Mateo &
Johnston 2000, 2003). Post-natal association with kin
was not necessary for this discrimination.
Olfactory learning of signature mixtures for famil-
iarization and phenotypic matching often occurs at
particular sensitive periods in life, a phenomenon
termed imprinting (explored in Chapter 9) (Hudson
1993). In mammals this tends to occur as a young
animal, say a young mouse pup in the nest learning the
odors, including those related to the MHC, and other
characteristics of its siblings in order to avoid them as
mates when adult (reviewed by Brennan & Kendrick
2006; Penn & Frommen 2010). Such learning has been
demonstrated by cross-fostering experiments with
young pups (if reared with a foster family, the pups
treat foster-family members as siblings) (see
Figure 3.10). Cues need only be a reliable statistical
indicator of kinship or group membership (Sherman
et al. 1997). As an adult, learning occurs with the
bonding with newly born offspring, as in the now
classic system of mother sheep and lambs (Chapter 9)
(Lévy & Keller 2009; Sanchez-Andrade & Kendrick
2009). It also occurs at mating in the female mouse,
which remembers the signature odor of its mate, pre-
venting pregnancy block (Chapter 9) (Brennan 2009).
The neonatal imprinting and odor-based recognition
of offspring occurs in humans too (Chapter 13) (Schaal
et al. 2009).
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Animals in a chemical world
Olfactory imprinting occurs in social insects
(Chapter 6). Ants, wasps, and bees learn their colony
odor after emerging as callow adults from their pupae
(Bos & d’Ettorre 2012; Breed 1998a; van Zweden &
d’Ettorre 2010). In ants, just as in mammals, the
learning can be demonstrated by cross-fostering a
pupa or newly emerged adult: the transferred ant will
learn the colony odor of its new hosts (Lenoir et al.
2001). Similarly, newly emerged Polistes wasps learn
the odors of the nest rather than their own odor.
However, individuals constantly need to reinforce and
fine tune their template with nestmate odors over time
(see below).
Some of these examples of individual or colony
recognition suggest there may be some selection for
receiver specialization for recognition (Tibbetts & Dale
ExamplesExperience Later recognition
Direct
familiarization
Territorial neighbo
r
(mammal)
Pairbond in
monogamous
mammals
Ground squirrels
A associates with B A and B recognize each other
Indirect
familiarization
2.
1.
Polistes wasps
MHC in mice
Ground squirrels
Beaver
a. Matching familiar
and unfamiliar kin
A associates with B A recognizes B* (close relative of B)
AA
A
A
B*
B
B
B
A
A
A*
b. Self-matching
(armpit or self-inspection)
Female cricket
mate choice
t-locus choice
in mice
Golden hamster
A becomes familiar
with self A recognizes A* (A and A* are kin)
A
ZnZ
Recognition-allele
green-beard system
3. Fire-ants for specific
genotype
Gp-9b vs Gp-9B
–
A (with allele Z) recognizes animal carrying
allele Z, whether or not kin, without learnin
g
no learning experience needed
Figure 1.9 Kin recognition mechanisms in almost all animals, vertebrates and invertebrates, seem to involve learning a signature
and then matching this template against the chemical profile of other animals. (The diagram is somewhat anthropomorphic as
mice do not have smelly armpits –but humans do.) Three mechanisms are represented:
(1) Direct
‡
familiarization, by learning the characteristics of nestmates and recognizing these animals later.
(2) Indirect
‡
familiarization (phenotypic matching): (a) learning the characteristics of nestmates and using the template to
allow phenotypic matching with unfamiliar kin; and (b) learning the odor of self to allow phenotypic matching of self with
others (self-referent or “armpit”phenotypic matching).
(3) Recognition allele (“green beard”). A (with allele Z) recognizes an animal carrying allele Z, whether or not kin, without
learning.
‡
Note: “direct”and “indirect”are used as by Porter and Blaustein (1989). The same words are used in a very different way by
other authors who use “indirect”for kin recognition rules using location e.g., “any baby in the nest is treated as kin,”compared
with “direct”for learning phenotypes, which would allow recognition away from the location, e.g., Pfennig and Sherman (1995)
and Waldman et al. (1988). Figure after Porter and Blaustein (1989) with modifications and additions. See Penn and Frommen
(2010) for more examples.
1.7 Chemical profiles and signature mixtures
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39
2007). This has been shown for visual recognition: a
species of social wasp, Polistes fuscatus, with visual
recognition of faces as the basis of colony hierarchy
has evolved a greater ability to differentiate between
wasp faces than a related species, P. metricus, which
lacks specialized face learning (Sheehan & Tibbetts
2011). It is likely that social insects have special parts
of the brain devoted to signature mixture recognition
and memory (Chapter 9).
Some of the examples of olfactory imprinting in
mammals, of young, and of mates (above), suggest
particular circuits or parts of the brain are involved (see
Chapter 9). However, mammals, includingourselves, are
also able to distinguish different individuals of another
species by smell, which suggests that some discrimina-
tions between conspecifics might rely on a general
ability to make distinctions between subtle differences
in complex mixtures rather than to perceptual mecha-
nisms specialized for conspecific odors (Johnston 2005).
For example, golden hamsters, Mesocricetus auratus,
and Djungarian hamsters, Phodopus campbelli,can
distinguish individuals of the other species (Johnston &
Robinson 1993). We do not know if they are learning
the same molecules as the other species would use, of
course (but then we do not know this for different
hamster individuals smelling conspecifics).
1.7.1.1 An exception to learned
recognition: greenbeards
The one theoretical exception that does not require
learning for kin recognition is the “greenbeard effect,”
proposed by Hamilton (1964) and named by Dawkins
(1976), with a hypothetical “supergene”or closely
linked genes with three effects that code (1) for a
conspicuous phenotype signal, (2) the genetic ability to
recognize it in others, and (3) a genetically determined
appropriate response. A greenbeard gene would
simultaneously give the owner a green beard and
prompt the greenbearded individual to look after
others with green beards (or harm those without one).
The first example found may be in the fire ant,
Solenopsis invicta: workers carrying one allele (Gp-9
b
)
of the supergene Gp-9 favor queens that share the
same allele (Gotzek & Ross 2007, 2009; Lawson et al.
2012a). The ant’sGp-9 supergene seems to make
workers carrying the Gp-9
b
allele kill non-carrier
queens (Gp-9
BB
) in multiqueen colonies. Gp-9 is a
marker for a linkage group of genes with no recombi-
nation, so it is yet to be resolved which genes in the
linkage group are responsible for the multiple observed
effects (Fischman et al. 2011; Lawson et al. 2012a;
Leal & Ishida 2008; Wang et al. 2008a). Cuticular
hydrocarbons may indicate queen Gp-9 genotype
(Eliyahu et al. 2011).
Greenbeard effects have also been found in the
social amoeba Dictyostelium, yeast, and lizards
(though chemical cues are not reported in the lizards as
yet) (see Gardner & West 2010; Penn & Frommen 2010;
West & Gardner 2010).
1.7.2 Which molecules are learned?
The signature mixture molecules in the chemical pro-
file, learned by receivers as the template for recogni-
tion, can be produced by the organism itself, acquired
from the diet, shared local environment, or other
organisms.
In mammals, genetically controlled cues produced
by the individual include odor cues related to the MHC
or lipocalin MUPs (Hurst 2009; Kwak et al. 2010).
Family members of badgers, Meles meles, also mark
each other with secretions during allomarking, when
they back up to each other and smear from their anal
and subcaudal glands (Buesching et al. 2003; Roper
2010, p. 198 ff.).
In many mammals, the fermenting of secretions by
microbes may provide some of the individually
varying odors (Archie & Theis 2011). For example,
which molecules are produced in our armpits is
affected by what we secrete and by which bacteria
thrive in our armpits (both are influenced by, for
example, the MHC, other genes, and factors such as
diet) (Chapter 13) (Figure 13.2) (Grice & Segre 2011;
Human Microbiome Project Consortium 2012). Males
of the neotropical greater sac-winged bat,
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Animals in a chemical world
Saccopteryx bilineata, appear to have individually
different odors coming from their fermenting wing
pouches and such differences may come from bacte-
rial species combinations that differ markedly
between individuals (Voigt et al. 2005).
The chemical profiles of mammal family groups
change as their diet and bacterial flora change. Some
of the exchanges of bacteria in family groups are
encouraged by behaviors such as allomarking by
badgers, Meles meles (above) (Buesching et al. 2003;
Roper 2010, p. 198 ff.). Marking behavior in hyenas
may have the same effect (Chapter 5) (Theis et al.
2012). A social insect colony’s shared label is also
constantly changing so the template has to be con-
stantly updated (Chapter 6) (Bos & d’Ettorre 2012; van
Zweden & d’Ettorre 2010). This constant change is
another reason for regarding signature mixtures as
different from pheromones.
In social insects, the colony chemical profiles are
determined partly by the insect’s own genes but also by
sharing molecules with other colony members, the
environment (e.g., nest, food, symbiotic fungi), or, in
some species, molecules from the queen (for more
detail see Chapter 6) (Breed & Buchwald 2009; Nash &
Boomsma 2008; Sturgis & Gordon 2012; van
Zweden & d’Ettorre 2010). Different taxa have char-
acteristic surface molecule types that vary and appear
to be involved in colony recognition: waxy molecules
in bees and CHCs in ants. Ant CHCs are typically
complex mixtures of alkanes, alkenes, and methyl
branched alkanes, and the number, weight range, and
chemical families of hydrocarbons differ between
taxa, including between species (Chapter 6) (Martin &
Drijfhout 2009a; van Wilgenburg et al. 2011). Within a
species, different colonies present different chemical
profiles based on the relative abundance of the same
genus- or species-characteristic components (Hefetz
2007; van Zweden & d’Ettorre 2010).
However, not all the CHCs on the surface of an ant
are involved in colony recognition. For example, the
CHC profile of the ant Formica exsecta is composed of
two independent parts: a colony-specific(Z)-9-alkene
profile under genetic influence and an
environmentally influenced task-related n-alkane
profile (Martin & Drijfhout 2009b). It is the ratio of
different (Z)-9-alkenes on an ant’s surface that is
“monitored”by other conspecifics to determine if it is a
member of the colony. The n-alkanes, which increase if
the ant has been foraging outside rather than working
underground, are disregarded in nestmate
recognition by the ants (Greene & Gordon 2003;
Martin & Drijfhout 2009b. (See Appendix for chemical
terminology and examples).
For nestmate recognition there may be selection
over evolutionary time for particular types of branched
hydrocarbons, which are easier to distinguish by shape
and offer the scope for more variation than straight-
chain hydrocarbons (Chapter 6) (this will in part be a
co-evolution with the receptor sensitivities of the
receivers, Chapter 9). Argentine ants, Linepithema
humile, learned to distinguish different tri-methyl
alkanes more easily than single-methyl or straight-
chain alkanes (van Wilgenburg et al. 2012). The ants
also found it easier to discriminate between hydro-
carbons with different branching patterns and the
same chain length, than between ones with the same
branching patterns but different chain length.
1.7.3 Is there selection for greater diversity in the
molecules offered in the chemical profile?
Most signature mixture-based recognition seems to
rely on co-option of variability that exists for another
reason (e.g., MHC) or has no selective advantage (e.g.,
diet). However, in the systems where the molecules in
the chemical profile are directly or indirectly under
genetic control (such as the ants, above) there might be
selection for greater diversity of molecules in the
“label”to allow greater distinctiveness either of indi-
viduals or of social insect colonies. An advantage for
visual distinctiveness, by for example reducing fights
because individuals are more easily distinguished, may
explain why, in Polistes paper wasps, only species with
complex social interactions have the variable facial
markings used in individual recognition (Tibbetts
2004; Tibbetts & Dale 2007).
1.7 Chemical profiles and signature mixtures
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41
Do social species have more complex chemical pro-
files? In mammals, an investigation of chemical com-
plexity of male and female glandular secretions in a
clade of eight related species of Eulemur lemurs sug-
gested greater complexity in species which live in
multimale–multifemale groups rather than in pair-
bonded species (delBarco-Trillo et al. 2012). The great
diversity of MUPs in the house mouse, Mus musculus
domesticus, may have been selected for in high-
density breeding populations with a higher chance of
encountering kin as potential mates (the polymorphic
MUPs can be used as a cue to reject mates sharing MUP
alleles with the chooser and thus likely to be kin;
Sherborne et al. 2007). In contrast, other mouse spe-
cies, such as Mus macedonicus, living at low densities
have only one MUP isoform in their urine (see in
Sherborne et al. 2007).
If the driver for selection for variety in the house
mouse polymorphous MUPs is mate choice (whether
the learned molecules are the MUPs themselves or
smaller molecules associated with them), the MUPs
could count as evolved signals rather than cues.
However, I would suggest that the need to learn the
variable MUPs (even for self-referent comparison) and
their great variety would have them count as contrib-
utors to signature mixtures in chemical profiles.
An indication that social insect species might have
more complex chemical profiles than solitary species
comes from almost 1,000 different hydrocarbons
found in just 78 ant species spread across 5 ant sub-
families (Martin & Drijfhout 2009a), which can be
contrasted with the 20 to 50 different hydrocarbons
typically found in non-social taxonomic families of
insects of all kinds (Chapter 6) (S. Martin, unpublished
data in Martin et al. 2008b). However, a stronger
comparison would be within hymeopteran groups,
such as halictid and allodapine bees, which show the
full range of social patterns from solitary to eusocial
among closely related species (Schwarz et al. 2007).
However, rather than selection for diversity, might
some of the diversity in hydrocarbon blends (labels)
between colonies come from a relaxation of the selec-
tion for conformity (i.e., permitting variation) in
contrast to the stabilizing selection for species recog-
nition signals that reduces deviation from a norm
(Chapter 3)?
1.7.4 How is diversity of chemical profile
maintained?
If molecules related to genetic labels are used for rec-
ognition of nestmates, whether in ants responding to
CHCs or family groups of mammals responding to
MHC odors, how is this diversity of labels maintained?
Genetic variability (polymorphism) in labels is
essential to allow distinction between nestmates and
non-nestmates. However, frequency-dependent selec-
tion against rare labels may remove label diversity from
recognition systems, leading to uniformity and making
distinction impossible, a situation known as “Crozier’s
paradox”(Penn & Frommen 2010; Tsutsui 2004) after
Crozier (1986, 1987). The selection against rare labels
could take the form of being rejected (for example,
being more likely to be seen as a non-nestmate and
prevented from re-entering the ant colony or a mammal
family’s burrow). Individuals that are less different from
the norm will havea selective advantage as they will be
less likely to be rejected as possible outsiders.
Crozier (1986, 1987) suggested that genetic marker
diversity used in recognition systems may be piggy-
backing on variation maintained by other forms of
selection such as parasites, pathogens, or mate choice.
This suggestion is supported by models of various
kinds (Gardner & West 2007; Penn & Frommen 2010).
In ants, greater diversity of CHC labels appears to occur
under greater parasite pressure (Chapter 11) (Martin
et al. 2011b). For mammals, the MHC is the basis of the
immune system and is under direct selection by para-
sites and disease (Chapter 3).
Mate choice to avoid inbreeding favors rarer genetic
markers, maintaining diversity. In the ant Leptothorax
gredleri, the cuticular hydrocarbons of both unmated
queens and reproductive males are colony specific and
this could in principle be used to avoid mating with
siblings (Oppelt et al. 2008). Similarly, in vertebrates,
mating choices for difference in the MHC may
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Animals in a chemical world
contribute to maintaining MHC diversity (Chapter 3)
(Milinski 2006). Similar arguments apply to MUPs in
mice (above).
1.8 Differences in response to pheromones
Different individuals may respond differently to the
same pheromone stimulus. While responses to phero-
mones are characterized by being “innate”(Section 1.2),
the responses can vary according to context, time of
day, and many other factors including the receiver’s
genetics, age, sex, hormonal state, dominance status,
and experience (Chapter 9). For example, honeybee
responses to alarm pheromone may depend on how
close to the nest they are (Chapter 9). Honeybee
responses to the many other honeybee pheromones also
change with age, as do the tasks undertaken (Chapters6
and 9) (Le Conte & Hefetz 2008). Different, overlapping,
subsets of the molecules give different messages
depending on the receiver (for example young or older
workers) and context (Box 6.3).
After mating, male Agrotis ipsilon moths stop
responding to female pheromone for up to 24 hours, the
time needed to replenish their accessory glands, though
their antennae still detect the female’spheromone
(Chapter 9) (Anton et al. 2007; Barrozo et al. 2010). Some
changes in response to sex pheromone are mediated
by responses to signature mixtures: animals do not
respondtootherwiseattractivesexpheromonesifthey
remember they have mated with that individual, recog-
nized by signature mixture (Coolidge effect) (Chapter 3).
1.9 Releaser and primer effects
of pheromones
Wilson and Bossert (1963) introduced the terms
releaser effects (immediate behavioral responses to
pheromones) and primer effects (longer lasting phys-
iological or developmental changes, sometimes medi-
ated by hormones). They recognized that some
pheromones had both effects. Later researchers tended
to refer to “releaser pheromones”and “primer phero-
mones.”It is clear now that the effects form a contin-
uum, so I think it is better to return to primer and
releaser effects rather than primer and releaser pher-
omones. There are many examples of pheromones or
their components having both kinds of effect at the
same time or one effect depending on the context or
receiver. Releaser effects may be accompanied by
longer lasting primer effects: the principal component
of honeybee alarm pheromone, isopentyl acetate,
elicits a quick defensive response from honeybees
(Chapter 8) and also induces gene expression in the
antennal lobes, perhaps underlying the lasting
changes in behavioral response to the pheromone
(Chapter 9) (Alaux & Robinson 2007; Alaux et al.
2009b). Similarly, the suckling response to rabbit
mammary pheromone by a rabbit pup (Box 1.5)
is accompanied by learning of maternal odors,
reflected in widespread immediate early gene activa-
tion in the rabbit pup brain (Charra et al. 2012;
Coureaud et al. 2010).
The male pheromones of mice, dehydro-exo-
brevicomin and 2-sec-butyl-4,5-dihydrothiazole appear
to have the releaser effects of eliciting aggression from
other males and attracting females, as well as the
developmental (primer) effects of apparently inducing
estrus in mature females and accelerating puberty in
young females (Chapter 9) (Novotny 2003). The honey-
bee queen’s mandibular pheromone attracts males
during her nuptial flight, a releaser effect, but when she
is queen of her own nest, the mandibular pheromone
plus additional components have the releaser effect of
attracting her retinue of workers around her (Chapters 6
and 9) (Grozinger 2013; Kocher & Grozinger 2011;
Slessor et al. 2005). The queen mandibular pheromone
also has a primer effect as a signal to the worker bees, her
daughters, that she is present and laying eggs (with the
physiological effect that the workers do not themselves
lay eggs). The multiple use of a pheromone within a
species for different functions is sometimes termed
pheromone parsimony (Section 1.4.2).
The multiple effects of a pheromone may act by
different receptors or nerve circuits. For example, the
1.9 Releaser and primer effects of pheromones
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43
modes of action of various primer and releaser effects
of different components of the honeybee queen man-
dibular pheromone on worker bees can be differenti-
ated experimentally (Chapter 9) (Grozinger et al.
2007a). Primer effects can be mediated via chemo-
sensory neurons such as olfactory sensory neurons or
by acting directly on tissues (Chapter 9) (Section 1.11).
Though the physiologies of mammals and insects are
very different, primer effects may work in similar ways
(see Chapter 9). For example, in mammals, dominance
hierarchies are reflected in blood gonadal hormone
concentrations (e.g., Saltzman et al. 2009). In social
insects juvenile hormone (JH) is often important in
pheromone-mediated effects (Alaux et al.2010;Le
Conte & Hefetz 2008).
While primer effects may act over days or longer,
some responses to endocrine-mediated pheromone
signals can be rapid. For example, the odors of estrous
female rats cause the release of hormones into the
blood in sex-experienced male rats, which give them
erections and elicit sexual behaviors within minutes
(Sachs 1999).
1.10 Multimodal signals
Multimodal signals involve more than one sense
(modality) and many include pheromones along with
sound or visual signals (Bradbury & Vehrencamp 2011,
pp. 296; Hebets & Papaj 2005; Partan & Marler 2005).
Signals may involve different modalities sequen-
tially (though some authors might not count this as
multimodal) (Partan & Marler 2005). Male butterflies
use visual cues to find females at long range and then
in many species, at short range they communicate with
pheromones (Chapter 3) (Allen et al. 2011). Many car-
nivores, such as dogs, add their scent marks to visually
conspicuous sites or landmarks. Ultraviolet (UV)
absorbing molecules in the scent marks of the desert
iguana, Dipsosaurus dorsalis, visually attract distant
conspecifics and once at the scent mark, the lizards
tongue-flick to pick up the non-volatile pheromone
molecules (Alberts 1990).
Some multimodal signals feature “redundancy,”in
which the signal in some modes can be omitted without
changing the message, as when we nod when speaking
the word “yes.”For example black-tailed deer alarm
signals are transmitted not only as an odor, but also as
sounds and visual signals (Chapter 8). Any one of
these may be effective in alerting other deer in the
group. This redundancy in signal can make dissecting
theroleofpheromonesmuchmoredifficult (Chapter 2).
Some multimodal signals are non-redundant. Male
Drosophila melanogaster fruit flies require a combi-
nation of chemical and visual stimuli from the female
for successful courtship; pheromones are necessary
but not sufficient alone (Chapters 3 and 9) (Dickson
2008). Some multimodal combinations can change the
meaning of signals. In the snapping shrimp, Alpheus
heterochaelis, male responses to visual threat signals
are changed if they are accompanied by female pher-
omones (Hughes 1996). There may be modulation of
the signal intensity by addition of other signals. For
example, in desert ant Aphaenogaster species,
recruitment of nestmates to a new food source is faster
when the scouts release pheromone and stridulate
(Chapter 7) (Hölldobler & Wilson 2009, p. 231).
Stimuli from different modalities are integrated in the
higher parts of the brain in both invertebrates
and vertebrates. For example, in the moth brain, neurons
integrate olfactory and visual inputs to give the motor
outputs for the flight response to a pheromone plume
(Haupt et al. 2010) (see also Chapter 10). In Crustacea,
hydrodynamic cues and chemical information are inte-
grated (Chapter 10) as are inputs from sensilla in both the
olfactory and distributed chemoreceptor systems
(Mellon 2012; Schmidt & Mellon 2011).
Stimulation in one modality can affect response in
another. Exposing male Spodoptera littoralis moths to
the ultrasonic clicks of predatory bats increases the
moths’behavioral response to female pheromone and
the sensitivity of central olfactory neurons in the
antennal lobe (Anton et al. 2011). Pup odors increase
the sensitivity of neurons in the primary auditory
cortex in mouse mothers to the ultrasonic distress calls
of pups (Cohen et al. 2011).
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Animals in a chemical world
The integrated inputs will be further modulated by
the animal’s internal state and experience, for example
the hormonal state of male hamsters affects their
responses to female odors (Section 1.8). An organism
in a natural setting interweaves signals from its
external and internal environment to yield an experi-
ence more complex than the sum of the individual
inputs (Stein & Meredith 1993).
The final outcome of semiochemical stimulation
comes from the integrated signals from the brain
prompting immediate behaviors, or changes over the
medium term such as increased alertness, or a com-
plete developmental switch affecting the rest of the
animal’s life as in phase change in locusts (Chapter 4)
(Section 1.9).
1.11 Allohormone pheromones bypassing
olfaction and taste
Some allohormone pheromones are passed directly to
another individual and have their effect directly on the
recipient’s tissues or sensory neurons but bypassing
the usual external sensory systems of taste and olfac-
tion (Chapter 9). This was anticipated by Karlson and
Lüscher (1959) in their example of termite pheromones
with primer effects on caste development, passed by
mouth around the colony (see Box 6.3). In honeybees,
nurse workers produce “royal jelly”containing an
allohormone pheromone, royalactin, which is fed to
larvae, switching them to develop as queens
(Chapter 9) (Kamakura 2011).
Hormones or other molecules may be directly
transferred by the male to the female when mating,
causing the female to reject other males; these include
prostaglandins in the semen of the red-sided garter
snake, Thamnophis sirtalis parietalis (Mason 1993),
and sex peptides in the seminal fluid of Drosophila
(Avila et al. 2011). The Drosophila sex peptide changes
the female’s behavior so that after mating she rejects
other males and starts to lay eggs (Chapter 3). The sex
peptide activates a specific receptor protein on specific
chemosensory neurons in her uterus and oviduct
(Chapter 9) (Häsemeyer et al. 2009; Rezával et al. 2012;
Yang et al. 2009).
The term allohormone was proposed by Koene and
ter Maat (2001, 2002) though Ruther and Steidle (2002)
argued against. I think allohormones, if the term is
seen to be useful, should be used as a subclass of
pheromone. Such an approach would allow us to avoid
classifying otherwise similar amphibian peptide pher-
omones differently depending on their route of trans-
mission: peptide pheromones are wafted in currents by
aquatic newt species, deposited on the openings to the
VNO in some terrestrial salamanders mating on land
(e.g., Plethodon shermani), and in most plethodontid
species, such as Desmognathus ocoee, applied trans-
dermally into the bloodstream of the female (via skin
scratches made with enlarged premaxillary teeth)
(Figure 1.7) (Section 1.4.3.3) (Houck 2009; Woodley
2010). The peptide delivered through the skin would
thus be an allohormone pheromone.
1.12 Pheromones and signature
mixtures in humans?
Sight and hearing are arguably our most important
senses, which probably make us different from many
other mammals. Nonetheless, olfactory signals and
chemosensory cues may be more important to us than
once supposed. For example, they may enable an
important part of the bond between parents and babies
and perhaps influence our choice of partner. However,
despite what is claimed in the wild west of the Internet,
no human pheromones have yet been properly
chemically identified and validated. These topics are
explored in Chapter 13.
1.13 Pollution disrupts chemical
communication in aquatic organisms
Aquatic organisms seem to be particularly vulnerable
to interference in chemical communication (“infodis-
ruption”) by human pollution (Lürling 2012; Olsén
1.13 Pollution and communication in aquatic organisms
|
45
2011; Zala & Penn 2004). Local effects include
endocrine-disrupting chemicals such as 17β-estradiol,
entering the environment via sewage outflows, which
has negative effects on male goldfish responses to
female pheromones. Invertebrates are also affected.
For example, crustacean male responses to female
odors are reduced by medetomidine, a molecule used
in antifouling coatings, or naphthalene from motor
boat fuel.
However, the most ubiquitous and global danger
probably comes from the atmospheric pollutant CO
2
through its effect on ocean acidity (Doney et al. 2009,
2012). Largely a result of human fossil fuel combus-
tion, CO
2
levels are rising at a rate about ten times
faster than has occurred for millions of years. About a
third of the CO
2
is absorbed by the oceans, reducing
their pH. If atmospheric CO
2
concentrations reach an
anticipated 800 ppmv by 2100 as predicted, the pH will
drop from the current and historic pH of between 8.15
and 8.25 to about 7.8 or below (Doney et al. 2009,
2012). This acidification is likely to have significant
effects on chemical communication by aquatic ani-
mals, which have evolved over 50 million years under
relatively constant pH levels.
Lowering the pH affects both the semiochemical
molecules themselves and their interaction with che-
mosensory receptor proteins. The way ligands (odor
molecules) interact with chemosensory receptors
changes with pH, as pH can affect the number, type,
and alignment of intermolecular forces (e.g., hydrogen
bonding, electrostatic potential, hydrophilic/hydro-
phobic regions) on both the chemosensory receptor
and the ligand (Hardege et al. 2011a; Kaupp 2010;
Reisert & Restrepo 2009). These include peptides,
nucleosides, thiols, and organic acids in nereid poly-
chaete worms; amino acids and peptides in Aplysia sea
hares; bile acids in fish; and nucleotides in crustaceans
such as shore crabs (Hardege et al. 2011a). For exam-
ple, many aquatic sex pheromones have acid dissoci-
ation constant (pK
a
) values in the range that is likely to
be affected by the lower pH values (JD Hardege, pers.
comm.). Experimental exposure to lower pH levels of
between 7.6 and 7.8, forecast to occur by 2100, did
indeed disrupt chemosensory responses of a diverse
range of species, from North Sea polychaete worms to
Caribbean shrimp species (JD Hardege, pers. comm.).
The disrupted pheromones and cues related to sexual
reproduction, feeding, sperm attraction, fertilization,
social interactions, and larval settlement. Vertebrate
chemical senses are also affected by lower pH: coral
reef anemonefish larvae, for example, no longer
respond appropriately to predator odors (Dixson et al.
2010). The fast rate of change of pH is likely to
outstrip the speed that chemosensory systems
can evolve.
Might the overall effects of lowering ocean pH be
the chemosensory equivalent of the blinding of the
world’s human population by a meteor shower at the
start of John Wyndham’s classic (1951) science fiction
novel The Day of the Triffids?
Summary
Across the animal kingdom, more interactions are mediated by pheromones and chemical
cues than by any other kind of modality. Many different kinds of compounds are used
as pheromones but there are many examples of the same compounds being used by
different species for different functions. Signature mixtures, learned as a template, enable
animals to distinguish each other as individuals or colony members. Pheromones tend to be
innate.
46
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Animals in a chemical world
The design of the olfactory system makes evolution of pheromones likely because there is
selection for any odor cue that increases reproductive success or survival. Thus pheromones
evolve from compounds originally having other uses or significance, for example from hor-
mones, host plant odors, chemicals released on injury, or waste products. Other signals may
evolve because they match previously existing sensitivities of the receiver. There is selection for
functional signal features such as longevity and specificity. There is also evolution in the senses
and response of the receiver. The original functions of the chemicals may or may not be
eventually lost.
There is less difference between vertebrates and invertebrates, in both the pheromones
produced and in the range of behaviors that pheromones influence, than was once thought.
Given the ubiquity of chemical communication among animals, pheromones and chemical cues
are likely to emerge as key criteria that animals use for mate choice.
The broad-brush diversity of pheromone molecules comes from the processes of evolving
from chemical cues, as molecules of all kinds are co-opted as signals. A finer grain of diversity
comes from the variations around a “chemical theme”as part of speciation. Multicomponent
pheromones of related molecules are often a result. The changes in pheromones that occur in
the process or speciation can involve large effects from a small number of genes or many genes
working together, or a combination of these.
Synergy describes the phenomenon when any one component of a multicomponent pher-
omone shows little or no activity by itself and only the complete mixture has an activity
comparable to the natural pheromone. It is to be expected from multicomponent pheromones
and may be a natural outcome of the combinatorial way they are processed in the brain of both
vertebrates and invertebrates.
Honest signals do not necessarily need to be costly and showing that a signal has a cost does
not demonstrate a handicap. Currently there is no experimental way of separately measuring
the two kinds of costs: efficacy (just to get the message out) and strategic (added costs for a
handicap). Signals can be kept honest by a variety of non-handicap mechanisms including
unfakeable indices, shared interest, and punishment of cheaters.
Acidification of the oceans due to rising carbon dioxide levels may seriously disrupt chemical
communication in aquatic organisms of all kinds because pH affects the interaction between
signal molecules and receptor proteins.
I hope that distinguishing between signature mixtures and pheromones (Table 1.1) could help
guide research strategies and help clarify what we have discovered so far. Karlson and Lüscher
(1959) ended their paper introducing “pheromones”by throwing the definition open for
discussion, saying that they hoped it would prove itself in practice, which 50 years on, it certainly
has. In a similar spirit, I welcome comments and suggestions for improving the ideas presented
in this book.
Summary
|
47
Further reading
For pheromones in particular taxonomic groups see Müller-Schwarze (2006) and chapters in East
and Dehnhard (2013) on vertebrates in general; Stacey and Sorensen (2011), Chung-Davidson
et al. (2011), and Sorensen and Wisenden (2014) for pheromones in fish; Hölldobler and Wilson
(1990, 2009) on ants and other social insects; Grozinger (2013) on honeybees; Allison and Cardé
(2014) on moths; and Hardie and Minks (1999) for other insects. Gaskett (2007), Schulz (2004)
and Trabalon and Bagnères (2010) cover various aspects of spider pheromones. Chapters in
Breithaupt and Thiel (2011) cover chemical communication in Crustacea in detail. Brönmark and
Hansson (2012) cover chemical communication in aquatic vertebrates and invertebrates.
Be aware when reading the past and current literature that the term “pheromone”is often
used ambiguously and may be used in contexts where “signature mixture”or “olfactory cues”
might be more accurate or helpful. Johnston (2003, 2005) gives a good overview of the ways
mammals use smell, in particular the way that individuals are recognized (describing “mosaic
signals,”which inspired the term “signature mixtures”).
For an excellent and comprehensive overview of communication see Bradbury and
Vehrencamp (2011), and also books by Maynard Smith and Harper (2003) and Searcy and
Nowicki (2005). However, for a fresh look at communication that challenges the “handicap”
mechanism, see Számadó (2011a,b).
The Nobel lectures of Richard Axel and Linda Buck offer clear, freely available, overviews of
how smell works (www.nobelprize.org) (Axel 2005; Buck 2005). For developments since then,
see Chapter 9.
For an insight into the diversity and molecular structure of pheromones, you can spend an
enjoyable and informative time browsing Pherobase www.pherobase.com developed and
maintained by El-Sayed (2013). See also the Appendix for a short guide to the terminology
(available for free download from the website associated with this book).
You can see the molecular structures of most molecules on sites such as www.chemspider.
com, which allows you to search by common name and shows synonyms as well as the
systematic names.
True to its title, this book focuses on animals. However, the social life of bacteria also involves
chemical communication, including quorum sensing, and is explored in a number of good
reviews including Keller and Surette (2006), Diggle et al. (2007), and Foster (2010).
48
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Animals in a chemical world
INDEX
Aardwolf. See Proteles cristata
Absolute configuration, 309
Acarosides (nematode pheromones)
potential use, control, 266
Accessory gland proteins (Acps), 88
Accessory olfactory bulb (AOB)
combinatorial processing, 179
Accessory olfactory system (AOS), 193
(5R,6S)-6-Acetoxy-5-hexadecanolide, 106
Acomys cahirinus (spiny mouse)
kin recognition cues, 131
Acromyrmex (leaf-cutter ant)
genetic CHC differences between patrilines, 130
Acromyrmex insinuator (ant), CHC insignificance, 257
Actias luna (silk moth)
antenna as sieve or paddle, 184
Active space, 227
Acyrthosiphon pisum (pea aphid)
alarm pheromone
ecological selection on response, 168
induces winged offspring, 169
suicide hypothesis, 168
Adoxophyes honmai (smaller tea tortrix moth), resistance to
pheromone control, 272
Aeolidia papillosa (nudibranch sea slug)
predator marked by prey pheromone, 167
Aethia cristatella (crested auklet, bird)
odor concentration & male rank, 75
African mole rats. See Heterocephalus glaber (naked mole rat)
Aggregation pheromones
Allee effects, 105
aposematic insects, 107
bark beetles, 107
larval pheromones, 108
definition, 105
dilution of risk, 105
ecophysiological benefits, 107
in space
feeding advantages, 110
for defense, 105
oviposition pheromones, 105–106
settlement of marine invertebrates, 109
reproductive benefits, 109
in time (synchronization)
barnacle egg hatching pheromone, 110
co-ordinating external fertilization, 69, 110
larval release, 110
intra-specific eavesdropping
males only signal until females arrive, 109
use in pest monitoring, 263
Agrotis ipsilon (black cutworm moth)
male response activated by juvenile hormone, 207–208
males stop responding to female pheromone after
mating, 43
Agrotis segetum (turnip moth)
regional variation in pheromone blend and co-varying male
receptors, 92
Ailuropoda melanoleuca (giant panda)
captive breeding, 262
male handstand, honest signal, 35
Alarm cues, 166–167
behavioral responses, 166
fish
“Schreckstoff”, 166
chondroitin, 166
hatchery trout learn predator odors, 262
neural circuits, 166
inter-specific responses, 166
public chemical information, 165, 166
survival benefits to responding, 166
use in pest management, 269
Alarm pheromones
alert signals, 165
aphids, 167
brain processing, 183
common lack of species specificity, 168
costs to responding
aphid drop, 168
diffusion from source, ants, 229
evolution from pre-existing chemical cues, 165, 170
evolution in unrelated individuals. See Alarm cues
fish. See Alarm cues; fish
larval insects in family groups, 165
multicomponent, 229
ant, 229
predator labeling with host pheromone, 167
propaganda, 251–258
social insects, 169–172
evolved from defensive molecules, 20–21
social species, 169
suicide hypothesis (aphids), 168
use for pest management, 270
Alcelaphus buselapus cokei (Coke’s hartebeest)
self-marking and presentation, 120
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Aleochara curtula (rove beetle)
she-male anti-aphrodisiac, 87
Alkaloids, 76
Alkylmethoxypyrazine, 107
Allee effects, 105
defense against predation, 105
definition, 105
ecophysiological benefits, 107
feeding, 110
for control, invasive pests, 267
for wildlife conservation, 262
mating, 109
external fertilization, 109
internal fertilization, 109
overcoming tree defenses
bark beetles, 107
Allelochemicals
definition, 6
Allocholic acid, 24
Allohormone pheromones, 45, 88–89, 213
Allomarking, 40, 132
Alloparental care, 130, 146, 219
egg dumping, 248–249
Allostatins, 212
Alpheus heterochaelis (snapping shrimp) modulation of visual
threat signals by female pheromones, 44
Alternative mating strategies, 86–87
eavesdropping parasitoids select for, 246
satellite males, 246
she males, 87
Altruistic behavior toward kin, 126
Alzheimer’s disease
sense of smell, loss, 283
Ambystoma tigrinum (tiger salamanders)
male condition vs. MHC, mate choice, 86
Amniotic fluid, 16, 130, 216, 282
Amphibians
alarm cues
tadpoles, learn predator odors and dangerous times
of day, 167
pest management (cane toad), 269
Amphid sensillae (nematodes), 210
Amphiprion spp. (anemonefish)
symbiotic with sea anemones, 249
Amygdala
integration of main olfactory and VNO outputs, 199–201
n-Amyl acetate, 185
Anastrepha ludens (fruit fly)
oviposition marking pheromone, 110
pest management, 269
Anastrepha oblique (fruit fly)
pest management, 269
Anastrepha suspensa (Caribbean fruit fly)
exaggerated signaling limited by predation, 37
lekking, 79
low cost of pheromone signaling, 34
Andrena nigroaenea (solitary bee), duped by
orchid, 252
Androstadienone (androsta-4,16-dien-3-one), 71
“putative human pheromone”, 296–299
perception, 294–295, 297–298
Androstenol (5α-androst-16-en-3α-ol), 290
“putative human pheromone”, 296–297
Androstenone (5α-androst-16-en-3-one)
“putative human pheromone”, 296–299
perception, 294–295, 297–298
Anemonefish and sea anemones, mutualism, 249–250
Animal welfare, 262–263
animal husbandry, 263
lab mice, 262
Anomala osakana (Osaka beetle), 25
Anonymous, pheromones, 7
Anosmias. See also under Humans:olfaction
specific, 293
Antagonists (inhibitors), 179
Ant-decapitating flies (phorids), 246
Anteroventral periventricular (AvPv) nucleus, 201
Anthonomus grandis (boll weevil)
low cost of pheromone signaling, 34
Anthopleura elegantissima (sea anemone)
alarm pheromone, 167
Anthopleurine, 167
Anti-aphrodisiac pheromones, 87–88
“chemical mate-guarding”,87
eavesdropped by parasitoids, 245
Antifouling coatings, 270
Ants
colony recognition, 129–130
enemy specification, 172
processing alarm pheromone, 183
queen pheromones
primer effects, 212–213
Aphaenogaster (Novomessor) (ant)
multimodal signals
recruitment for foraging, 44
recruitment, 157
Aphaenogaster cockerelli (ant)
queen detects cheating workers, 37
Aphids
alarm pheromones, 167–169
(E)-β-farnesene, 168
ecological selection on response, 168
induce winged offspring, 169
not species specific, 24
social species, 169
suicide hypothesis, 168
use for pest management, 270
sex pheromones (multicomponent, species-specific), 24
Apis cerana japonica (Japanese honeybee), 170–171
co-ordinated defense against hornet, 170–171
Index
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Apis mellifera (honeybee)
alarm pheromone
immediate and longer term effects, 208
anarchistic colonies, 142, 214
bee-keeping
using pheromones to manage swarms etc, 260
blending of colony odor on comb wax, 128
brood pheromone, 136, 145, 214
effects on worker nurse–forager transition, 214–215
cell capping, pheromones, 136, 145
colony odor sources, 128
colony recognition, 127–128
complexity of pheromones in colony, 134
control of worker reproduction
maintaining, 214
differences between queens and workers, 213
gene expression, 214
larval pheromomes
E-β-ocimene, 214
multiple paternity in nest, 128
olfactory receptors
AmOR11, male receptor for 9-ODA, 62
large number of different, for an insect, 189
pheromone responses change with age, 43
hormones underlying, 208
pheromones lead to changes in worker bee brain gene
expression, 62, 172
pheromones summary, 142–145
queen mandibular pheromone (QMP), 142, 214
as sex pheromone, 135
effects on worker nurse–forager transition, 214–215
multiple signals, parsimony, 25
primer effects, 43
rapid colony response to loss, 141, 144
releaser effects, sex pheromone, 43
swarming, 145
transmission, 141, 144
queen pheromones
mechanisms, 213–215
queen retinue pheromone (QRP), 142
recruitment pheromones with waggle dance, 155
response to QMP depends on early exposure, 16
royal jelly, 45, 144, 213
royalactin, 45, 213
RNAi used in discovery, 60
worker nurse–forager transition, 214–215
changes in brain gene expression, 214
worker task allocation behavior related to forager and malvolio
gene expression, 215
Aplysia (sea slug)
oviposition pheromones, 105
peptide sex pheromones, 23
Apocephalus paraponerae (phorid fly), eavesdrops host alarm
pheromone, 246
Aposematic insects
aggregation pheromones, 107
Applications of semiochemicals
animal husbandry
biostimulatory effects, 261
primer effects, 271
animal welfare, 262–263
beneficial insects
bumblebees, 260
honeybees, 260
captive breeding rare species, 262
commercialization, challenges to, 272–273
greenhouse IPM, virtuous spiral, 263
pest management
alarm cues, 269
alarm pheromones, 270
deterrent odors, 269
lure and kill or mass trap, 266–269
marine antifouling, 270
mating disruption, 264–266
combined with biological control, 266
mechanisms, 264
monitoring, 263–264
pest resistance to pheromones, 272
primer effects, 271
push–pull (stimulo-deterrent diversionary) strategies, 270
self-protecting plants, 270
slow–release formulations, 264
trail pheromones, 270
Aquaculture, 262
pollution risk, from, 262
Arabidopsis thaliana (plant)
transgenic, producing aphid alarm pheromone, 270
Arginine vasopressin, 218
Argyropelecus hemigymnus (deep-sea hatchet fish), mate
location, 223
Armpit effect (self-inspection or matching), 38
Arms race, 258
Arrestment, 107, 224, 270
Arthropodin (settlement-inducing protein complex, SIPC), 109
Artificial insemination (AI)
use of Boarmate
TM
, 261–262
Ascarosides (nematode pheromones)
multicomponent, identification, 58
Assembly pheromone
ticks, 107
Assortative mating (like with like), 90
Asymmetric tracking, 94
Atta leaf-cutter ants, trunk trails, 158
Atta texana (ant)
sensitivity of workers to trail pheromone, 154
Atta vollenweideri (leaf-cutter ant)
trail pheromones
macroglomerulus in worker brain, 183
sensitivity to, 154, 230
Axillary malodor releasing enzyme (AMRE), 289
380
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Bacteria. See Microbes
Bactrocera dorsalis (oriental fruit fly)
adult feeding key to male success, 75
Badgers. See Meles meles (European badger)
Badges of status, Nauphoeta cinerea (cockroach), 72
Balanus balanoides.See Semibalanus balanoides
Bark beetles. See also Aggregation pheromones; Allee effects;
Dendroctonus; Eavesdropping; Ips
aggregation pheromones
evolved from detoxification of tree defenses, 20
climate change leading to tree stress and beetle epidemics, 107
larval aggregation pheromones, 108
mass attack, 107
mass trapping, 266
Barnacles
disrupting settlement, 270
egg hatching pheromone, 110
larval settlement, 52, 109
transcriptome studied, 62
Beavers. See Castor
Begging, 36
Benzaldehyde, 255
Benzyl cyanide, 88, 245
Bet-hedging
marine larval settlement, 110
Bicyclus anynana (butterfly)
male pheromones and mate choice, 99
Bioassays. See also Semiochemical identification
appropriate concentrations, 53–54, 179
behavioral analysis software, 53
brain imaging, 55
functional magnetic resonance imaging (fMRI), 55, 199,
297, 299
optical, 55
positron emission tomography (PET) scans, 55, 297, 299
challenges for
demonstrating individual recognition, 132–133
identification and synthesis must include
stereochemistry, 25
learning, 277
multicomponent pheromones, 54–55
multimodal signals, 54
non-physiological concentrations, 298
randomization and blinding, lack of, 53
replication, lack of, 53
signal redundancy, 54
chemical profiles and signature mixtures, 52–53
direct manipulation of chemical profiles, 53, 127
distinguishing individuals, 52
principal components analysis, 53
recognition, aggression bioassays, 53
ecological relevance, 50
electrophysiology, 55
does not always predict behavioral response, 55
electroantennogram (EAG), 55
electro-olfactogram (EOG), 55
electrovomerogram (EVG), 55
single cell recording (SCR), 55
humans
organoleptic tests, 289
T-shirt sniff tests, 278
loss-of-function mutants as tool, 50, 58
multicomponent pheromones
subtractive method, 54–55
olfactometers, 54
primer effects, 51
standardization, necessary but problematic, 51
test details can affect results, 51–52
aggression bioassay in ants, 53
discrimination vs. habituation task, 51
lab animal strain, 51
prior experience and learning, 51
Biomarkers, 58
Biostimulatory effects, livestock, 261
Birds
chemical profile differences in related species, 91
cryptic female choice, 85, 89
eavesdropping vole scent marks by ultraviolet cues, 245
major histocompatibility complex (MHC)
mate choice, 84, 85
mate choice by odor, 75
olfactory receptor (OR) gene repertoire similar to mammals,
189
preen gland, 57
semiochemicals, 3
tracking plumes, 227, 242
uropygial gland secretions differ between the sexes, 66
Blattella germanica (cockroach)
uses CHC profiles to avoid sibs, 81
Boarmate
TM
, 261, 262, 263
Body condition, 19, 36, 75, 76
Bombus (Psithyrus)bohemicus (cuckoo bumblebee), 258
Bombus (Psithyrus) spp. (cuckoo bumblebee), 257
Bombus spp. (bumblebees)
footprints on flowers, 111
Bombus terrestris (bumblebee)
foraging recruitment pheromone, 155, 260
Bombykol, 2, 49, 55
Bombyx mori (silk moth), 2, 184
Bos taurus (cattle)
estrus detection, 261
Bostrichthys sinensis (black sleeper fish)
aquaculture, 262
Boundary layer, 228, 229
effects on sense organ design, 184
flick and sniff to mitigate, 186
Bourgeonal, 298
Brain imaging, 55
functional magnetic resonance imaging (fMRI), 199,
297, 299
Index
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Brain imaging (cont.)
optical, 55
positron emission tomography (PET) scans, 55, 297, 299
Brainbow (visualizing neural circuits), 62
Brevicomin, 24
Bruce effect, 133, 146, 219–221
does it occur in wild?, 220
Bufadienolide toxins, 269
Buteo lagopus (rough-legged buzzard)
visual eavesdropping, 245
n-Butyl-n-butyrate, 139, 212
2-sec-Butyl-4,5-dihydrothiazole, 11, 27, 193
Caenorhabditis elegans (nematode)
aggregation pheromones, 105
ascarosides, 58
dauer pheromone, 25
primer effects, 210–211
metabolomics to identify multicomponent pheromones, 58
orientation behavior, 226
pheromonal parsimony, signal meaning depends on
concentration, 25
selection for change in dauer pheromone receptor at high
density, 190
sex pheromone
multicomponent, 25, 28
Callinectes sapidus (blue crab)
orientation in plume, 239
Callithrix jacchus (common marmoset)
subordinate female ovulation suppressed, 146
Camouflage. See Deception
Camponotus floridanus (ant)
alarm pheromone, brain imaging, 183
colony recognition, processing in brain, 216
queen pheromone passed round colony on queen’s eggs, 141
Camponotus japonicus (ant)
sensilla involvement in colony recognition, 216
Camponotus obscuripes (ant)
alarm pheromone, brain imaging, 183
Camponotus socius (ant)
group recruitment, 153
Cane toad. See Rhinella marina
Canis lupus (grey wolf)
border marks in territory, 121
Canis lupus familiaris (domestic dog)
“dog-appeasing pheromone”, 262
detectors
estrus, cows, 261
human disease, 283
distinguishing humans by smell, 278
female advertisement pheromone, 66
female sex pheromone, still unidentified, 5
forensic use of smell, 282
nasal flow design for olfactory sensitivity, 186
olfactory sensory sensitivity, compared to human, 185
track trails and detect direction, 233
Canis sinensis (Ethiopian wolf)
border marks in territory, 121
Capra aegagrus hircus (domestic goat)
male effect, 201, 221
males mark females when mounting, 124
Carassius auratus (goldfish)
chemical duets to co-ordinate external fertilization, 69
combinatorial processing of multicomponent
pheromones, 179
endocrine-disrupting pollution affects response to
pheromone, 46
multicomponent sex pheromones, 27
primer effects, bioassay, 51
scramble competition, 70
Carboxylic acids, 290
Carcinus maenas (crab)
mate guarding of pre-molt female, 71
priming effect of female pheromone,
sensitizes, 207
Cardiocondyla obscurior (ant)
alternative strategies, wingless males with mandibles and
females mimic males, 87
Castes. See also Ants; Apis mellifera; Social insects; Termites
development, 207, 211–213
differences
brain structures, 183, 207
pheromone secretions, 32, 135
responses to pheromones, 169, 171
self-organization models for proportions of different castes, 163
specialist soldier-guards to resist robber bees, 255
Castor canadensis (beaver)
anal glands, 120
avoids marks at low population densities, 115
castoreum gland, 120
kin recognition, 120, 131
over-marking, 120
pest management, 264, 269
scent-matching, 120
territories
scent matching hypothesis, 120
Castor fiber (Eurasian beaver)
territories, scent-matching, 120
Castoreum, 120
Cataglyphis niger (desert ant), territories “owner
advantage”, 116
Cats. See Felis catus
Cattle. See Bos taurus
Central-place foragers, 150
Ceratitis capitata (Mediterranean fruit fly)
benefits of female choice unclear, 81
eavesdropped by predator, 245
cost to signaling, 37
leks, 79
used as pheromone decoys, 264
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Ceratovacuna lanigera (social aphid)
soldiers, 169
c-fos, 218
Chemical profiles
definition, 2
do social species have more complex?, 41–42
how diversity maintained, 42–43
identification. See Semiochemical identification
mate choice, MHC, 82
social insects and social mammals, 126
Chemical senses
compared with other senses, 4
Chemosensory receptors
contrasted with opsins, 4
evolution, 188–192
“birth-and-death”process, 189
independent in insects & vertebrates, 188, 195–197
opportunistic co-option, many receptor families, 188
selection on receptor repertoire and sensitivities, 189
insects
gustatory receptors (GRs), 197
ionotropic receptors (IRs), 197
odorant receptors (ORs), 196
unrelated to vertebrate receptors, 196
use ionotropic signaling pathways, 196
mammals
all receptor types are GPCRs, 192
formyl peptide receptors (FPRs), 195
trace amine-associated receptors (TAARs), 192, 193
vomeronasal receptors (V1Rs and V2Rs), 192, 193–195
Chemosensory systems
invertebrates and vertebrates
taste (gustation) vs. smell (olfaction), 175
Chiloglottis spp.(orchids)
speciation, 253
Chiloglottones (2,5-dialkylcyclohexan-1,3-diones), 253
Chiral molecules, 25, 306
Chocolate trails, humans follow, 233
Cholesta-5,7-dien-3-ol (provitamin D
3
), 21
5β-Cholestan-3-one, 152
Chondroitin, fish alarm cue, 166
Cimex lectularius (bed bug)
aggregation pheromone
monitoring, 263
alarm pheromone, pest management, 270
arrestment by pheromone, 224
cis-regulatory DNA, 29, 91
cis-trans isomers, 310
Citral, 255
Cleptobiosis, 255
Cleptotrigona (stingless bee), uses propaganda pheromones, 255
Clethrionomys glareolus (bank vole)
females prefer odors of dominant male, 75
Climate change
ocean acidification, 46
tree stress and bark beetles, 107
CNV. See Copy number variation
Coccinelidae (ladybugs)
detect larvae, lay fewer eggs, 111
Coccinella septempunctata (ladybug)
aggregation pheromone, 107
Cockroaches
aggregation
ecophysiological benefits, 107
sex pheromones
highly varied between genera, related within, 28
Co-evolution
social parasites and host social insects, 255–258
Colletes cunicularius (solitary bee), duped by orchid, 252
Colony level selection, 214
Colophina monstrifica (social aphid)
soldiers, 169
Communication, 18, 32 See also Pheromones; Signals
Composite signals. See Signals; multimodal
Concentration
pheromonal parsimony, 24–25
signal meaning depends on, 24–25, 54, 157, 210
too high, response specificity lost, 53, 54, 179
Conservation
captive breeding, 262
using scent marking to manipulate mate choice, 262
vertebrate scent marks to census, 263–264
Contact chemoreception, 175
Coolidge effects, 86
mechanisms, 218
Co-operative breeding, 146, 219
Copulatory plug, 23, 88, 89
Copulins, 299–300
Copy number variation (CNV), 191, 292
Coremata, 66, 76
Corpora allata, 139, 207, 212, 214
Cortisol, 89, 279
Corynebacteria, 288
Corynebacterium striatum, 289
Cosmophasis bitaeniata (spider)
gets colony-specific CHC from host ant, 257
Cosmopolites sordidus (banana weevil)
aggregation pheromone, for control, 266
Costs (of signaling). See Signals, costs
Countermarking. See Over-marking
p-cresol, female horse pheromone, 261
Critical periods
behavioral development, 16
caste development, 213
Crocuta crocuta (spotted hyena)
scent marking patterns, variation by habitat, 121
Cross-fostering, 85, 131
social insects
sources of colony odors, 128
species-specific mate recognition, 16
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Crotalaria (plant), source of alkaloids, 76
Crozier’s paradox, 42
Crustaceans
aggregation for defense, 105
antennal flicks (sniffs)
scaling with increasing size in lifetime, 186
avoiding predator odors, 248
distributed chemosensory system on claws, 175
individual recognition, 72
mediated by aesthetascs pathways, 215
larval settlement from plankton, 109
lobster flicks antennae to smell, 186
male lobsters fight for ownership of shelters, 72
mate guarding, 71
orientation behavior
copepods following pheromone trails, 230
crabs orienting in odor plume, 239
integration of olfactory and hydrodynamic cue inputs, 44
pheromones
contact sex pheromones (copepods), 8
metabolomics may be fruitful approach to identification,
58
modulation of visual threat signals by female
pheromones, 44
uridine diphosphate, shore crab female pheromone, 71
pollution
chemosensory disruption from ocean acidification, changes
ligand interaction, 46
male responses to female odors are reduced, 46
symbiosis with sea anemones, 250
synchronized larval release, 110
transcriptome studied, 62
Cryptic choice, 89–90
Cryptotermes secundus (termite)
differences in gene expression, queens vs. kings and workers,
139
queens and nymphs, different CHC profiles, 138
Cues
definition, 18
Culex (mosquito)
oviposition pheromone, 24, 106
Cuticular hydrocarbons (CHCs), 155
camouflage, 257
deception, 255–258
foragers’CHCs different vs. workers inside nest, 41, 130
social insects
colony odors, sources, 41
colony recognition, 126–130
Cydia pomonella (codling moth)
pest management, 264
Cynictis penicillata (yellow mongoose)
scent marking, 114
Cynops ensicauda (newt)
peptide pheromone, 25
Cynops pyrrhogaster (red-bellied newt)
peptide pheromone, 25
population differences in male peptide pheromone, 92
species-specific male peptide pheromone, 91
Cyprinus carpio (common carp)
multicomponent sex pheromones, 27
pest management, 267
Cypris larvae (barnacles), 52, 109
Cysteine-glutathione, 70
Danaus gilippus (queen butterfly)
male transfers pheromone direct to female, 23
Darcin (mouse Mup20), 35
binds 2-sec-butyl 4,5 dihydrothiazole (thiazole), 219
interaction of pheromone and signature mixture, 219
prompts learning male signature mixture and location, 16,
118, 124, 209, 219
Darwin, Charles
sexual selection on pheromones, 5, 65
Dauer larva Caenorhabditis elegans (nematode), 25,
210–11
Dear-enemies (territorial defense), 118, 123, 133
Decanal, 75
Decapod shrimps
mate guarding, 71
Deception, 251–258
aggressive chemical mimicry, 251–258
blister beetle, 253–255
bolas spiders, 251
pollination by sexual deception, 252–253
imperfect mimicry more attractive, orchid, 252
aided by shared biochemistry in all life, 244
ants and lycaenid butterflies (see also Mutualism),
250
code breaking, 244
cost of not responding to deceivers, 251
mechanisms (insignificance, chemical camouflage, chemical
mimicry), 250
of social insects, 255–258
arms race, 258
camouflage, 257
chemical insignificance, 257
counterfeiting, 257
Decyl acetate, 255
Deer. See Odocoileus hemionus columbianus
Dehydroepiandrosterone, 290
Dehydro-exo-brevicomin, 27, 193, 210
Dendraster excentricus (sand dollar)
feeding currents, benefits of aggregation, 110
planktonic larval settlement, 110
Dendroctonus (bark beetles)
Dendroctonus brevicomis, eavesdropped by
predators, 246
Dendroctonus frontalis, 108
Dendroctonus micans, 108
larval aggregation pheromones, 108
384
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Dendroctonus ponderosae, 107
Dendroctonus pseudotsugae, 108
Dendroctonus rufipennis, 107
Dendroctonus valens, 108
Desaturase enzymes, 94
Desaturase 1 gene, 101
Desmognathus ocoee (Ocoee salamander)
transdermal transfer of pheromone to female bloodstream, 45
Development
caste differences in social insects pheromone production and
perception, 207
effects on response to pheromone, 207
learning
maternal behavior, 216
response to semiochemicals, 16
sensory system, periphery, 16
social control of reproduction
social insects and social mammals, parallels, 147–148
switch
dauer pheromone, 25, 210–211
social insects, 45, 211–213
Diaeretiella rapae (parasitoid wasp), arrested by aphid alarm
pheromone, 270
Diastereoisomers, 309, 310
Dictyostelium (slime mold)
greenbeards, 40
Differential analysis by 2D-NMR spectroscopy (DANS), 58
2-(sec-Butyl)-dihydrothiazole, 210
1,5-Dimethyl-6,8-dioxabicyclo[3.2.1]octane (frontalin), 11
Dimethyl disulphide, 283
4,8-Dimethyldecanal, 89
2,5-Dimethylpyrazine, 193
Dinoponera quadriceps (ant)
alpha female badge, 7
Diomedea exulans (albatross)
navigation, food location, 226, 242
Dipsosaurus dorsalis (desert iguana)
multimodal signal with ultraviolet cue, 44
scent marks with ultraviolet cue, 123
Disassortative mating, 85
Disruptive selection, 94
DNA methylation, 213, 215
Dodecadienol, 157
Dodecatrienol, 157
(Z)-7-Dodecen-1-yl acetate, 11, 24
Dodecyl acetate, 255
Dogs. See Canis lupus familiaris
Dolichotis patagonum (mara), males directly urine mark
females, 124
Dopamine, 16, 142, 218, 219, 221
Doublesex (dsx), 101, 201–204
Drosophila grimshawi (Hawaiian fruit fly)
benefits of female choice unclear, 81
Drosophila melanogaster (fruit fly)
adult flight behavior, 226, 240
changes in CHCs with age, 57
cis-vaccenyl acetate (cVA), anti-aphrodisiac, 22, 88, 179, 202
forager and malvolio gene expression, comparison in
honeybee, 215
gustatory (as well as olfactory) receptors for pheromones, 175
males, response to CHC pheromones, 15
larval orientation behavior, 226
learning
discriminating receptive partners, 204, 209
macroglomerular complex, 181
male adjusts ejaculate and mating time vs. sperm competition, 89
multimodal courtship signals, 44, 54, 201–204
olfactory receptors
polymorphisms, 191
regional races differ in CHC blends, 92
sex peptide, 45, 88–89, 204
sex-specific neural circuits, 201–204
Drosophila melanogaster subgroup
rapid speciation
cuticular hydrocarbons, 99–103
Drosophila sechellia (fruit fly)
cuticular hydrocarbons in species isolation, 103
olfactory binding proteins and taste responses, 198
Drosophila serrata (fruit fly)
speciation, involves more than sexual selection
alone, 90
Drosophila simulans (fruit fly)
cuticular hydrocarbons in species isolation, 103
repelled by Morinda citrifolia (plant), 198
Dufour’s gland
host-marking by parasitoids, 111
Dulotic ants, 255
Eavesdropping, 244–249
aggregation pheromones, 246–248
ant alarm pheromones, 246
arms race, 247
egg dumping, 248–249
intra-specific
hormones evolving into pheromones, 18
sex pheromones as aggregation pheromones, 68, 105, 107,
246, 248
of predator odors by prey, 248
sex pheromones, 245–246
“bridge-in-time”, 245
territorial markings, 246
Ecdysteroid hormones, 89, 139, 212, 213
Eciton (army ants), foraging models, 161
Efficacy cost, 32
Egg dumping, 248–249
Eicosanoids. See PUFAs
(Z)-11-Eicosen-1-ol, 21, 80
Elater ferrugineus (beetle), monitor for rare prey, 263
Electronic noses, 283
Elephants. See Elephas maximus;Loxodonta africana
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Elephas maximus (Asian elephant)
detects pheromones in female urine, 71
dominant males and musth, 76
pheromones shared with moths and beetles, 24
Elminius modestus (barnacle), long penis, 109
Enantiomers, 25, 306
Endocrine-disrupting chemicals, 46
β-Endorphin
Ephestia elutella (tobacco moth)
females choose larger males, 75
Epidermal club cells, 166
Epidermal growth factor receptor (EGFR), 213
Epigenetic effects, 62, 106, 213
Epiphyas postvittana (light brown apple moth)
pest management, 264
Epistatic interactions, 98, 103
(3Z,9Z)-(6S,7R)-Epoxy-heneicosadiene, 251
Equus caballus (horse)
female sex pheromone, p-cresol, 261
Esox lucius (pike)
prey learn to associate odor with alarm cue, 167, 262
17β-estradiol, 46
Estratetraenol, “putative human pheromone”, 297
Estrous cycle synchrony
doubts, 210
4-Ethyl-2-methoxyphenol, 72
Ethyl oleate, 142, 145, 214
Ethyl palmitate, 145, 214
4-Ethyloctanoic acid, 290
Eucalyptol, 155
Euglossine bees
collect species-specific plant perfume oils as pheromone, 31
Eulemur spp. (lemurs)
greater complexity of glandular secretions in more social
species, 42
Euproctis taiwana (moth), 245
Eusociality. See also Social insects; Social mammals
conflict over reproduction in societies, 136–137
continuum (reproductive skew), 136
co-operative broodcare, 136
social insects and social mammals, parallels, 147–148
Evolution. See Pheromones, evolution
Evolvability, 191
Exocrine gland-secreting peptide 1 (ESP1), 11, 179, 184, 194,
204–206
Expectancy violation, mate choice, 78
Experience. See Development; Learning
Experimental methods. See Semiochemical identification
E-Z isomers, 310
Fabre, Jean-Henri, 5
Falco tinnunculus (kestrel)
visual eavesdropping, 245
(α)-Farnesene, 210, 270
(E)-β-Farnesene, 24, 168, 210, 255, 270
Fat body, 213
Felis catus (domestic cat)
“feline facial pheromone”(Feliway
TM
), 262
flehmen, 193
odors invoke fear in rats, 248
Female choice. See Mate choice, Sexual selection
Fertility signal, 36, 137–146
Fish
androgen effects on electro-olfactogram (EOG), 207
brain
neural circuits for response to alarm cues, 166
processing of pheromones, 187
chemosensory disruption from ocean acidification, changes
ligand interaction, 46
internally fertilizing, cryptic female choice, 89
learn predator odor association with alarm cue, 167, 262
male pheromones, 66
males advertise parental care, 77
orientation behavior
lateral line, use in rheotaxis, 241
rheotaxis, 241
tropotaxis, 242
pheromones
evolution, 19
for management of invasive species, 267
multicomponent, 19
sexual selection and imprinting, 74
sniff, 186
tracking plumes, 226, 241–242
Fixatives
2-phenoxyethanol, 23
fatty acid esters, 23
Flavor, 175, 278, 302
Flehmen, 193
Flicks, antennal
behavior of smelling, 186–187
scaling with increasing size in lifetime, 186
Fluctuating asymmetry, 81, 300
Follicle-stimulating hormone, 89, 199
Foraging (for) gene, 215
Formica ant spp.
formic acid as defense and alarm pheromone, 21, 170
Formica cunicularia (ant), propaganda victim, 255
Formica exsecta (ant)
CHCs in colony recognition, 127
colony-specific cuticular hydrocarbons, 13, 41
Formica fusca (ant)
diversity of CHCs driven by social parasitic ants, 258
Formica japonica (ant)
colony odor successfully synthesized, 15
Formica lemani (ant), host to syrphid fly, 258
Formica subintegra (slave-making ant), use of
propaganda, 255
Formicoxenus (shampoo ant), social parasite of Myrmica
ants, 257
386
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Formyl peptide receptors (FPRs), 78, 195
co-option from immune system, 188
Fright reaction. See Alarm cues, fish
Frontalin, 76
Fruitless (fru), 201–204
GABA, 216–217
Galaxias fasciatus (banded kokopu fish), lateral line for
rheotaxis, 241
Gallus gallus (red junglefowl)
cryptic female choice, 89
Gammarus roeselii (crustacean), avoids predator odor, 248
Gargaphia solani (aubergine lace bug)
intra-specific egg dumping, 248
subsocial care, alarm pheromone, 165
Garter snake. See Thamnophis sirtalis parietalis
Gas liquid chromatography (GC). See Semiochemical
identification
Gasterosteus aculeatus (stickleback, fish)
mate choice
diversity of MHC optimized, 85
major histocompatibility complex (MHC), 85
Gasterosteus spp. (sticklebacks, fish)
imprinting, basis of sexual isolation of two species, 16, 74
GC. See Semiochemical identification
Gene expression, 214
brain
induced by pheromone exposure, 208
differences related to roles in honeybee workers, 214–215
Genomics
RNA-seq, 62–63
sociogenomics, 212
Geometrical isomers (cis-trans, E-Z), 310
Geranial, 255
Geraniol (3,7-dimethylocta-2,6-dien-1-ol), 165
Gestalt model
colony odor, 127, 128
Giant panda. See Ailuropoda melanoleuca
Glands
anal, 77, 120, 132
areola
humans, 295
castoreum, 120
cephalic, 80
Dufour’s, 37, 129, 142, 255
humans
apocrine, 287
apoeccrine, 287
areola, 295
eccrine, 287
sebaceous, 287
sweat glands, 287–288
hypopharyngeal, 213
labial, 155
mandibular, 142, 213
metatarsal, 167
post-pharyngeal, 129
pre-orbital, 121
pre-putial, 210
pygidial, 153
salivary, 145
social insects
summarized, 134
sternal, 129
subcaudal, 132
temporal, 76
tergal, 142, 155
van der Vecht, 170
venom, 212
Glutamic acid, 70
Glycoprotein
barnacle, 109
GnRH pulse generator, 201
Gobius niger (fish)
chemically inconspicuous sneaker males, 87
Gonadotropin-releasing hormone (GnRH) neurons, 199–200
Good genes, 75
G-protein-coupled receptors (GPCRs), 192
Grapholita molesta (oriental fruit moth)
flight track, 240
Greenbeards, 40 See also Recognition
Grueneberg ganglion, 195
Gryllodes sigillatus (cricket)
Coolidge effect, 86
Guaiacol (2-methoxyphenol), 31
Guanine, 107
Guanylate cyclases, 188
Gustation
compared with smell (olfaction), 175
olfactory binding proteins
specificity of response, 198
Gustatory receptors (GRs)
insect GRs
“pickpocket”ion channels, 203
ionotropic (unrelated to vertebrate GRs), 197
Gustatory sensory neurons (GSNs)
insects, 197
Gynandromorphs, 201
Habituation
aphids, to alarm pheromone, 270
Habronestes bradleyi (spider), attracted to
fighting ants, 246
Habropoda pallida (solitary bee), duped by blister
beetle larvae, 253
Hamilton, selfish herd, 249
Hamilton’s rule, kin selection, 133, 145
Handicap theory, 32, 33–34, See also Signals
immunocompetence handicap hypothesis, 79
reliable signals without handicap, 32–37
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HapMap, 281
Hawaiian drosophilid speciation, 91–92
Headspace sampling, 57
Heliconid butterflies
anti-aphrodisiacs, 88
Heliconius charithonia (butterfly)
males guard female pupae, 71
Heliconius melpomene (butterfly)
male pheromones
fixative extends signal life, 23
Helicoverpa armigera (cotton bollworm moth)
seminal fluid molecules, 89
Helicoverpa zea (corn ear worm moth)
sensitive to sympatric species’pheromone components, 55
Heliothis subflexa (moth) and Heliothis virescens (tobacco
budworm moth)
directional pressures on pheromone blends in sympatric
species, 90
male pheromones in courtship prevent hybrid matings, 97–98
polygenic divergence in signal and male detection in
sympatric species, 29, 97–98
Heliothis virescens (tobacco budworm moth)
flight track, 240
seminal fluid molecules, 89
Helogale undulata (dwarf mongoose)
individual recognition, 132
can discriminate anal gland secretions, not cheek
gland, 133
(3Z,6Z,9Z)-Heneicosatriene, 251
9-Hentriacontene, 7
7,11-Heptacosadiene, 88, 100, 203
2-Heptanone, 193, 194, 199
Herpestes auropunctatus (Indian mongoose)
individual recognition, 132
Heterocephalus glaber (naked mole rat)
colony odor, parallels with social insects, 132
queen suppression of worker reproduction, by physical
dominance, 146
recruitment of foragers, 155
Heterodera glycines (soybean cyst nematode)
pest management, 266
(Z,E)-7,11-Hexadecandienyl acetate, 305
(Z)-9-Hexadecenal, 270
Hexanoic acid, 290
Hexenoic acid, 290
(Z)-3-Hexen-1-ol (cis-3-Hexen-1-ol), 295
Hexyl decanoate, 155
Hidden preferences (receiver psychology), 21
High performance liquid chromatography (HPLC), 55
Homarus americanus (lobster)
contest, 72
flicks antennae to smell, 186
pre-copulatory mate guarding, 71
Homo sapiens.See Humans
Homovanillyl alcohol (HVA), 142
Honest signals. See Signals
Honeybees. See Apis mellifera
Hormones. See also Primer effects
cortisol and recognition, human mothers, 279
definition, 6
influence on central/peripheral responses to
pheromones, 207
male body condition
mate choice by females, 75–76
primer effects, 43–44
similarities between mammals and insects, 43
social insect caste development, 139
testosterone androgen effects
male hamster brain needs to respond, 208
Horse. See Equus caballus
Host-discrimination, 110
Host-marking pheromones (HMP)
evolution of, 111
host-discrimination, 110
individual recognition, 111
Human leucocyte antigen (HLA). See Humans, mate choice;
Major histocompatibility complex (MHC);
Mammals
Humans (Homo sapiens)
advertisement of ovulation?, 299–300
“copulins”, 299–300
male ability to detect, 300
age, changes with
perception, 283
secretions, 284
androstadienone (androsta-4,16-dien-3-one)
perception, 294–295, 297–298
androstenone (5α-androst-16-en-3-one)
perception, 294–295, 297–298
anosmias
many molecules induce changes on
exposure, 298
antiperspirants and deodorants
modes of action, 289
sales, 282
areola glands, 295
axilla (armpit) hair and odor-creating
bacteria, 288
chemical profiles and signature mixtures
mate choice, 280
mothers and babies, 278–279, 282
cleanliness not necessarily a virtue, 282
earwax and armpits, 290–291
estratetraenol
“putative human pheromone”, 297
follow chocolate trail, 233
genetic polymorphisms, 291
perception of smell, 292–295
smell production, 290–291
mammary pheromone?, 295
388
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mate choice
body symmetry, 300
evidence from 250 years’data, Iceland, 84
kibbutz or Westermarck effect, 280
major histocompatibility complex (MHC), 279–284
oral contraceptives, effects?, 281
steroid “putative human pheromones”, 296–299
T-shirt sniff tests, 281
microbes
contribution to odor, 288–290
variation over body and between people, 288–290
mother–infant olfactory recognition, 217
mothers and babies
areola gland secretion, mammary pheromone?, 295
mother cortisol and baby recognition, correlation, 279
recognition, 278–279, 282
odor preferences
genetics, olfactory receptor variation, 292–295
learning, 277
foods, 277
neonates different from older children and adults, 277
odors and memory
experimental tests, 280
Proust, smells bring back memories, 280
odors, cultural and social aspects, 277–278
Napoleon, 277
osmologies, 303
perfumes, 277
sexual attraction, 277
olfaction, human
anosmias
specific, 292–295
compared, dogs, 185
compared, mice and primates, 275
distinguishing isomers, 309
genetic polymorphisms, 191, 278, 292–295
loss, color vision hypothesis, 291
olfactory bulb, size, 275
unique individual worlds, 191, 278, 292
primer effects
menstrual synchrony?, 300–301
recognition, 278–279
children, sibs, parents, 279
mother–child, 278–279
phenotypic matching, 279
security blankets (comforters), 279
self, partners, 279
T-shirt sniff tests, 278
sexual orientation, 287
signature mixtures, 278
steroid “putative pheromones”, 10, 54, 296–299
androstadienone, 296–299
androstenol (5α-androst-16-en-3α-ol),
296–297
sweat glands
apocrine, apoeccrine, eccrine, 287–288
odorless precursors, 290
using human odors
forensics, 282
problems, 282
mammary pheromones, 282
medical diagnosis, 283
smell loss, neurodegenerative diseases, 283
smells produced by disease, 283
dogs as detectors, 283
electronic noses, 283
mood changers and “aromatherapy”, 283
vomeronasal organ (VNO), vestigial, 291
Hutterites, MHC and partner choice, 281
Hyaena brunnea (brown hyena)
pasting marks, 123, 132
Hyaena hyaena (striped hyena), social
greeting, 123
Hydrobates pelagicus (storm petrel, bird)
avoid kin as mates, 84
Hydroides (marine worm)
larval settlement, bet-hedging, 110
Hydroquinone (1,4-dihydroxybenzene), 158
3-Hydroxy-2-butanone, 72
(E)-10-Hydroxy-2-decenoic acid, 135, 213
6-Hydroxy-6-methyl-3-heptanone, 193, 210
3-Hydroxy-3-methyl-hexanoic acid, 290
Hyperosmias, 293
Hyposmias, 293
Iberolacerta cyreni (lizard)
male pheromones depend on body condition, 36, 75
pre-existing sensory bias, food lipids, 21
Ichneumon eumerus (parasitoid wasp), uses propaganda,
255
Iguana iguana (lizard)
male femoral gland stimulated by testosterone, 75
Immunocompetence handicap hypothesis, 79
Imprinting, 38–40
can lead to sexual isolation of two species, 16, 74
definition, 215
similarities between mammals and social insects, 129
species-specific mate recognition, 16
Index signals, 35
Indices (unfakeable signals), 35–36
Individual recognition, 38, 72, 118, 132, 133
challenges for, demonstrating, 132–133
Indole, 88
Infochemicals, 6
Infodisruption by pollution, 45
Information, 18, See also Pheromones; Signals
Innate behavior, 16
Inosine, 70
Insect vectors, 263, 270
Insulin signaling, 139, 211, 212
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Integrated pest management (IPM), 263, 264
push-pull (stimulo-deterrent diversionary) strategies, 270
Interaction between modalities, 44
Interspecific interaction, semiochemical mediated. See
Deception; Eavesdropping; Mutualisms
Ips pini (pine engraver bark beetle), 246
Ipsdienol, 246
Iridomyrmex purpureus (ant), alarm pheromone attracts spider,
246
Isomers, 305–310
biological importance, 49, 246, 304
chiralty, 306
human smell distinguishes, 309
naming conventions, 309
(-/+), (d/l), (D/L), 305, 307
absolute configuration, (R), (S), 309
optical, 307
racemic mixture (racemate), 307
stereoisomers (spatial isomers), 306
diastereoisomers (not mirror images), 309
enantiomers (mirror images), 306
structural (constitutional), 305
chain, 305
functional group, 305
geometrical isomers (cis-trans, E-Z), 310
positional, 306
Isopentyl acetate, 43, 208
Isovaleric acid (3-methylbutanoic acid), 294
Ixodes neitzi (tick)
responds to scent marks of host antelope, 246
Ixodes scapularis (tick), clusters on host deer trails, 246
Jacobson’s organ. See Vomeronasal organ (VNO)
(R)-Japonilure, 25
(S)-Japonilure, 25
Juvenile hormone (JH), 34, 89, 139, 212, 213, 214, 215
Kafue lechwe (Kobus leche, antelope)
lekking, 80
Kairomones, 136, 166, 244–249
Kalotermes flavicollis (termite)
sex differences, 138
Kangaroos
mate guarding by male, 71
Keifera lycopersicella (tomato pin worm)
pest management, 266
3-Keto petromyzonol sulphate, 22
15-Keto-prostaglandin-F
2α
, 207
Kibbutz or Westermarck effect
human mate choice, 279
Kin selection, 36, 37, 133
Kinesis, 224, 225
Kisspeptin, 200–201
Kobus kob (Uganda kob, antelope)
lekking, 80
Labeled line, 179, 183
Lacerta monticola.See Iberolacerta cyreni
Lacinipolia renigera (moth)
victim of bolas spider, 251
Ladybugs. See Coccinelidae
Lanierone, 246
Lasioderma serricorne (cigarette beetle)
aggregation pheromone, 109
Lasioglossum zephyrum (sweatbee)
guard bees discriminate relatedness, 128
Lasius alienus (ant)
panic response to its alarm pheromone, 171
Lasius fuliginosus (ant), 255
Lasius neoniger (ant)
co-operative foraging, 153
Lasius niger (ant)
marking behavior on colony home range, 160
modeling foraging, 160
queen marking of eggs, 146
queen pheromone, 3-methylhentriacontane (3-MeC
31
), 141
queen pheromones, 213
Lateral protocerebrum, 183
Learning. See also Development
alarm cues
gives flexibility of response, 167
hatchery trout learn predator odors, 262
discriminating receptive partners, 204, 209
family and kin recognition
mammals, 130–133
mammals
maternal ewes bond quicker on subsequent births, 209, 217
needed to distinguish estrous from diestrous female
odors, 209
mitral cells in main olfactory bulb, 216–217
parasitoid insects
generalist learns host pheromones, 245
sensitive period, 131, 216
signature mixtures, 38–41, 215–218
Lee–Boot effect, 210
Leks, 79–81
Lemur catta (ring-tailed lemur), “stink fights”, 113, 114
Lepomis cyanellus (green sunfish), alloparental
care, 248
Leptogenys peuqueti (ant)
multicomponent trail pheromone, 28, 157
Leptothorax acervorum (ant)
tandem running recruitment, 153
Leptothorax gredleri (ant)
colony-specific CHCs may help inbreeding
avoidance, 42
Lestrimelitta (stingless bee), uses propaganda pheromones for
cleptobiosis, 255
Lévy walks, 226
Limonene, 31
Linalool, 71
Linalool oxide (furanoid), 71
390
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Linepithema humile (Argentine ant)
bioassay design affects aggression result, 53
learning to distinguish branched CHCs easier, 41
trail pheromone, disrupting, 270
Linyphia litogiosa (spider), conflict between the sexes, 69
Lipaphis (Hyadaphis) erysimi (aphid)
alarm pheromone, 168
Liriomyza sativae (leafminer fly)
pest management, 266
Litoria splendida (magnificent tree frog)
male pheromone, peptide, 66
low cost, 34
L-kynurenine, 23
Locust. See Schistocerca gregaria
Loligo pealeii (squid)
aggressive contests, prompted by egg mass protein
pheromone, 72
Lordosis, 206, 261
L-Ovothiol-A, 70
Loxodonta africana (African elephant)
dominant males and musth, 76
mate guarding, 71
Lure and kill, pheromone control, 266
Luteinizing hormone, 89, 199
Lutzomyia longipalpis (sandfly)
lekking, 79
Macrotermes (termite)
building queen chamber, 163
nest building, 161
Maculinea alcon (Alcon blue butterfly)
arms race of deception, 258
Maculinea rebeli (lycaenid butterfly), 255
Major histocompatibility complex (MHC)
familial imprinting, 218
odor preferences for difference in mates, 85
human leukocyte antigen (HLA), 280
humans
mate choice
evidence from 250 years’data, Iceland, 84
interaction with individual’s microbial flora, 82
kin recognition, 84
mate choice, 81–86, 279–284
for greater diversity of MHC alleles, 85
MHC diversity, 85
mutual distinguishing MHC of odors in rats, mice, and
humans, 280
not always found in wild populations, 85
self-reference, 85
preferences
women taking oral contraceptives, 281
selection for polymorphism to avoid inbreeding?, 42
selection pressures maintaining diversity of MHC alleles, 84
disassortative mating, 281
greater resistance to disease or parasites, 85
higher implantation rates if dissimilar, 85, 281, 284
reduced chance of inbreeding if dissimilar, 85
sources of the odors, 82
Major urinary proteins (MUPs)
add longevity to volatile signal, 23
cue to avoid inbreeding, 218
darcin (Mup20) (mouse), 124, 219
high metabolic cost of use in scent marking, 35
mate choice, inbreeding avoidance, 86
mice
dominant males, 118
Male effect (goats and sheep), 201, 221
Malvolio gene, 215
Mammals. See also Humans; Primates; Social mammals
family and kin recognition, 130–133
clan or group, 131–132
individual recognition, 132–133
kin, 131
mother–offspring, 130–131
learning
needed to distinguish estrous from diestrous female odors,
209
pheromones, 12
primer effects, 209–210
scent marks to census, 263–264
Man. See Humans
Mandrillus sphinx (mandrill)
no estrous synchrony found, 210
Manduca sexta (tobacco horn moth)
octopamine influences peripheral response to
pheromone, 207
sexual dimorphism, antennae, receptors, brain, behavior, 201
Mastophora hutchinsoni (bolas spider)
aggressive chemical mimicry of moth pheromones, 251
Mastotermes darwiniensis (termite)
labial gland pheromones, 158
Mate choice
benefits, 73
body condition, 35–36
effect via testosterone, 75
by males, 76
fluctuating asymmetry, 81, 300
for health/avoid infection, 77–79
genetic compatibility, 81–86, 279–284
imprinting, 74
leks, 79–81
major histocompatibility complex (MHC), 81–86, 279–284
mechanisms
“runaway sexual selection”(“Fisherian sexy sons”), 74
antagonistic coevolution (chase-away sexual selection), 74
compatible genes, 74
direct benefits, 74
importance of learning/imprinting, 74
indicators, 74
interaction with environmental factors, 74
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Mate choice (cont.)
operational sex ratio, 73
overview, 73–75
paternal investment, 76–77
quality signals, 75–76
to avoid inbreeding
familial imprinting, 218
Mate guarding. See Sperm competition and mate guarding
Maternal behavior and recognition, 130–131, 278–279
Medial amygdala
integration of individual identity cues from
VNO and MOE, 216
Medial pre-optic hypothalamus (MPOA)
sensitization by experience, 209
testosterone androgen effects
male hamster brain needs to respond, 208
Meles meles (European badger)
clan recognition, 132
latrine distribution, variation by habitat, 123
scent marking, potential population management, 269
squat marking (allomarking), 40, 132
Meloe franciscanus (blister beetle), triungulin larvae, 253
Menstrual synchrony, 300–301
p-Menth-1-en-8-ol, 302
Mesocricetus auratus (hamster)
contribution of different glands to individual odor,
generalizations, 133
female advertisement, vaginal secretion trails, 66
learning own identity from litter mates, 38
recognition of individuals of other hamster species, 40
Messor barbarus (harvester ant)
matching trail patterns to food distribution, 159
Metabolomics, 57–58, 301
Methoprene, 34
Methyl linolenate, 214
3-Methylbutanoic acid (isovaleric acid), 294
2-Methyl-1-butanol, 139, 212
2-Methylbut-2-enal, 11, 25, 55
Methyl 4-methylpyrrole-2-carboxylate, 154
Methyl eugenol, 75
(Z)-16-Methyl-9-heptadecenyl isobutyrate, 245
4-Methyl-3-heptanol, 246
4-Methyl-3-heptanone, 229, 246
(R)-(-)-5-Methyl-3-heptanone, 70
(S)-(+)-5-Methyl-3-heptanone, 70
6-Methyl-5-hepten-2-one, 246, 255
Methyl ketones, 76, 84
Methyl oleate, 145
Methyl palmitate, 145
Methyl salicylate, 88
3-Methylhentriacontane (3-MeC
31
), 141
2-Methylthiazolidine, 72
(Methylthio)methanethiol, 11, 187, 199
MHC. See Major histocompatibility complex
Mice. See Mus musculus domesticus
Microarrays, 62
Microbes
contribution to odor
effect of MHC variation, 82
human odors, 288–290
mammals, individual and clan odor, 40, 132
changes over time, 132
fish, antimicrobial secretions to protect eggs, 77
quorum sensing, 48
Microdon mutabilis (syrphid fly), matches its ant host, 258
Micromys minutus (harvest mouse)
captive breeding, using scent marks, 262
Microtus ochrogaster (prairie vole)
partner recognition, 133, 218
recognition of family males prevents pick up of male
pheromones by female juveniles, 147, 219
Microtus pennsylvanicus (meadow vole)
adjusts ejaculate if sperm competition likely, 89
male scent glands graded response to testosterone, 75
males on better diets, more attractive, 36, 75
Mimicry. See Deception
Minimal-cost signals, 36
Mitral/tufted (M/T) cells, 183, 187
involvement in memory, 216–217
Modulation of response to pheromones and multimodal inputs, 45
Monomorium minimum (ant), mass recruitment to exclude
competitors, 157
Monomorium pharaonis (Pharaoh’s ant)
multiple trail pheromones, 160
role specialization, trail laying, 160
trail polarity, 233
Morinda citrifolia (plant)
host to Drosophila sechellia, 198
Morpholino oligonucleotides, 60
Mosaic signal, 6, 10
Mother–infant recognition, 130–131
Moths
male pheromones
host plant molecules, evolved via sensory exploitation, 99
multiple independent evolution, 99
male scramble competition, 69
pheromones
behavioral antagonists, 95
brain wiring flipped in species using opposite ratios of same
molecules, 97
multicomponent, male response wider than range females
produce, 29
multicomponent, redundancy, 54
overview, 94–96
preventing cross-attraction between sympatric species
time of day, host plants, blends, 95
saltational shifts, 29
signal change in speciation, 28–30
synergy as natural consequence of combinatorial
processing, 28
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whole blend acts at a distance, 27, 95
Mouse. See Mus musculus domesticus
Multicomponent pheromones, 19
alarm
social insects, 170
challenges to identification, 54–55
definition, 25
male response wider than range females produce, 29
mechanisms for evolutionary change of blends, 31
synergy, 210
inevitable outcome of combinatorial processing, 28
whole blend acts at a distance, 27, 95
Multimodal signals. See Signals, multimodal
Mungos mungo (banded mongoose)
nasty neighbors, 123
over-marking and mate choice, no evidence, 124
Mup20. See Darcin
Mus macedonicus (mouse)
little MUP diversity vs. high density living house
mouse, 42
Mus musculus domesticus (house mouse)
contests for ownership of territories, 72
co-operative breeders, 146
darcin, 219
estrus induction and puberty acceleration in females
(Whitten & Vandenbergh effects), 209–210
exocrine gland-secreting peptide 1 (ESP1), 204–206
familial imprinting, odor preferences for difference in
mates, 85
individual recognition, 118, 132
major histocompatibility complex (MHC)
selection for polymorphism to avoid inbreeding?, 42
major urinary proteins (MUPs)
add longevity to volatile signal, 23
darcin, prompts learning male signature mixture and
location, 16, 118
haplotype, cue to avoid inbreeding, 218
high metabolic cost of use in scent marking, 35
mate choice, inbreeding avoidance, 86
male pheromones, 72
mate choice
MHC diversity, 85
MHC related odors, 82
multicomponent male mouse pheromone, 27
Peg3, paternally imprinted gene, odor learning, 209
pup odors increase mother response to pup ultrasonic distress
calls, 44
pups learn individual odor cue of mother as cue for
suckling, 66
scent marking, 118
as reliable signal of territory ownership, 35
darcin, 118
marking rates, dominants and subordinates, 118
mate choice, 118
punishment of subordinates if challenge scent marks of
dominant, 37
reduce cleaning for lab animal welfare, 262
response varies by competitive ability, 118
subordinates do not secrete pheromones, do not scent mark, 87
territories
over-marking
freshness, mate choice, 124
scent matching hypothesis, 117–118
Mus musculus subspecies (mouse)
divergence in odors, 90
Mushroom body, 183, 207, 216
Mustela erminea (stoat)
anal gland secretions repel herbivore prey, 269
Mustela putorius furo (ferret)
sex differences in response to pheromones, 206
Mustela vison (American mink)
scent baited traps, 263
Mustelus canis (dogfish), plume tracking, 226
Musth. See Elephas maximus;Loxodonta africana
male elephants, 76
Mutualism, 249–250
ants and lycaenid butterflies (see also Deception), 250
aphids tended by ants, 250
egg dumping as, 248
sea anemones and anemonefish, 249–250
Myrmecia gulosa (bulldog ants)
cheating workers imobilized, 36
Myrmica rubra (ant)
host to lycaenid butterfly, 258
Myrmica sabuleti (ant)
matching foraging effort to food value, 160
Myrmica schencki (ant), 255
Myzus persicae (aphid)
response to alarm pheromone, 270
Naked mole rats. See Heterocephalus glaber (naked mole rat)
Nasogenital grooming, 219
Nasty neighbors, 123
Nasutitermes (termite)
soldiers, alarm pheromones, 171
Nasutitermes takasagoensis (termite)
queen-specific volatiles, 139
Natural selection, definitions, 65
Nauphoeta cinerea (cockroach)
body condition as reliable signal, 35
body condition reflected in pheromones, 75
male contest and female choice, 72
silent satellite males, 87
Near-infrared spectroscopy (NIRS), 57
Nematodes. See also Caenorhabditis elegans
multicomponent pheromones
ascarosides, 27
parasitic, potential control, 266
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Nematodes (cont.)
pheromones for pest and disease management, 266
sex pheromones, 266
Neocapritermes taracua (termite), suicidal defense, 171
Neocembrene, 157, 304
Neofem2, 139
Nepotism, 128, 131
Neral, 255
Nereis succinea (polychaete worm)
pheromones co-ordinate external fertilization,
70, 110
Next generation sequencing (NGS), 62–63
Nicrophorus defodiens (burying beetle)
conflict between the sexes, 69
Nicrophorus vespilloides (burying beetle)
Coolidge effect, 86
Niveoscincus microlepidotus (lizard), partner recognition, 133
Noise, 95, 178
Noradrenaline. See Norepinephrine
Norepinephrine
release in olfactory bulbs
learning, 216–217
Notropis umbratili (redfin shiner fish) inter-specific egg
dumper, 248
Nuclear magnetic resonance (NMR) spectrometry, 58
Nycticebus pygmaeus (pygmy loris)
captive breeding, 262
over-marking, female choice, 124, 262
Ocean acidification
dangers to whole ecosystem by interference with
chemosensory systems, 46
(E)-β-Ocimene, 23, 145, 214
Octanal, 75
Octopamine, 89, 207, 208
Octyl decanoate, 155
Odocoileus hemionus columbianus (black-tailed deer)
alert signals, 165
Odor space, 174, 193
Odorant binding proteins (OBPs), 198
specificity of response
gustation, 198
Odorants
can be any size, 173
Oecophylla longinoda (African weaver ant)
alarm pheromone response, 229
recruitment systems, 150
territories
‘owner advantage’, 116
Oecophylla smaragdina (weaver ant)
territories, nasty neighbors, 123
Oleic acid, 36, 75
Olfaction. See also Gustation, humans
accessory olfactory bulb (AOB)
combinatorial processing, 179
amygdala
integration of main olfactory and VNO outputs, 199–201
behavior of smelling (sniffs and flicks), 186
combinatorial coding, 173, 178–181
compare lateral inputs, 233, 240
eavesdroppers as sensitive as legitimate target, 244
genetic polymorphisms, 191, 292–295
glomeruli, 176
links to higher levels of brain, 186
no simple chemotropic map, 178
similarity in vertebrates and insects, 176–178
insect macroglomerular complex (MGC)
moth male brain, 179
processing of many pheromones is without, 181–183
size reflects OSN numbers, 181
integration of olfactory and hydrodynamic cue inputs, 44
integration of olfactory and visual inputs, 44
integration of vertebrate olfactory systems, 198–201
labeled line, 179, 183
main olfactory system (MOS)
functional overlap with vomeronasal olfactory system
(VNO), 198–201
mapping brain activity
fluorescing dyes, 183
odorant-binding proteins (OBPs), 197
odorants
can be any size, 173
olfactory bulb
modulation
by lateral interactions, 183
top–down input, 185
olfactory cortex
compare lateral inputs, 233
olfactory receptors. See Olfactory receptors
olfactory sensory neurons (OSNs). See Olfactory sensory neurons
one neuron –one receptor, 177
possible separation between general olfaction and pheromone
processing, 187
projections to higher brain, 183–187
response to predator odor, 187
temporal coding in brains, 187
fast oscillations, synchronization, 187
vomeronasal olfactory system (VNO)
functional overlap with main olfactory system (MOS), 198–201
Olfactory cortex, 183
Olfactory organs
functional design, 185
sensitivity thresholds compared, dogs, humans, 185
sensitivity thresholds compared, mice and primates, 275
Olfactory receptor co-receptor (ORCO) (OR83b), 197
Olfactory receptors (ORs). See also Gustatory receptors (GRs)
binding sites, 179
investigated by site-directed mutagenesis, 179
evolution
“birth-and-death”process, 189
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inhibitors (antagonists), 179
insects
co-expressed with olfactory receptor co-receptor (ORCO), 197
unrelated to vertebrate receptors, 196
use ionotropic signaling pathways, 196
mammals
evolvability facilitated by glomerular development
mechanisms, 190
odorant binding sites, 190
odorant characteristics, 179
pH changes ligand interaction, danger from ocean
acidification, 46
tuning and specificity, 176, 178–181, 190, 191, 292
Olfactory recess, nasal flow design for sensitivity, 186
Olfactory sensory neurons (OSNs)
odorant effects on development, honeybee, 16
renewal (mammal), 191
Oncorhynchus masou (masu salmon)
female sex pheromone, L-kynurenine, 23
Oncorhynchus mykiss (rainbow trout)
learn predator odor, 262
Oncorhynchus tshawytscha (salmon)
MHC mate choice prevented by male harassment, 85
Ondata zibethicus (muskrats) monitoring, 264
Ontogeny. See Development
Ophrys exaltata (orchid)
dupes solitary bee
imperfect mimicry more attractive, 252
Ophrys sphegodes (orchid) dupes solitary bee, 252
Optimal outbreeding, 84, 252
Optogenetics, 60
OR11H7P, 294
OR1D2, 298
OR2J3, 295
OR7D4, 294
OR83b (olfactory receptor co-receptor, ORCO), 197
OR912–93, 193
Orchids
pollination by sexual deception
aggressive chemical mimicry, 252–253
ORCO, 197
Orconectes rusticus (crayfish)
distributed chemosensory system on claws, 175
Oreochromis mossambicus (tilapia, fish)
urine release by dominant males during contests on leks,
72, 79
Oreotragus oreotragus (klipspringer antelope)
scent marks eavesdropped by ticks, 246
territories, 121
economics of scent marking, 121
Oriental fruit moth. See Grapholita molesta
Orientation behavior
active space, 227
diffusion, 227–229
arrestment, 224
chemical plumes, 223
response to odor filaments, 238
chemical specificity, 223
combining information from different senses,
230, 241
crustaceans, 238
directly guided (taxis), 224, 225
idiothetic, 224
indirectly guided (kinesis), 224, 225
insects
tracking plumes, 240–241
mechanisms, 223–226
kinesis, 224, 225
klinokinesis, 224, 226
orthokinesis, 224
optomotor anemotaxis, moths, 240
taxis, 224, 225
chemotaxis, 230, 239
klinotaxis, 224, 225, 226, 230, 239
rheotaxis, 241
teleotaxis, 224
tropotaxis, 224, 225, 230, 231, 232, 239, 242
odor “landscape”, 223
odor concentration gradient, 225
odor stimulus
plumes, 235–242
short range diffusion, 227–229
trails, 229–235
pheromones allow low-density species to find mates,
223
ranging, 226–227
crosswind, 226
Lévy walks, 226
scale, 223
self-steered, 224
counter-turning
moths, 240
teleology, 223
trails, detecting direction of
ants, 233
copepods, 230
dogs, 233
snails, 233
snakes, 233
stingless bees, 233
upwind orientation by male moths, 179
stop if wrong species, 179
Oryctolagus cuniculus (rabbit)
chinning, marking behavior, 114
fixatives extend signal life, 23
mammary pheromone, 11
prompts learning other odors, 16, 209
Osmetrichia, 66
Osmia rufa (red mason bee)
chooses mates from own population, 84
Index
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Osmoderma eremite (scarab beetle), rare species monitored via
predator, 263
Ostariophysi, 166
Ostrinia furnacalis (Asian corn borer moth)
reconstructing speciation events, 29, 97
Ostrinia nubilalis (European corn borer moth)
E & Z strains also isolated by male pheromones, 99
older male pheromones attractive, 76
pheromone signal genetics, 29, 30, 96–97
Ourebia ourebi (oribi antelope)
territories, group defense, 121
Over-marking, 120
mate choice, 118, 123–124, 262
Oviposition pheromones, 106
Schistocerca gregaria (desert locust), 106
Oviposition-marking pheromone (OMP). See Host-marking
pheromone (HMP)
Ovis aries (sheep)
male (ram) effect, 221
use in animal husbandry, 261
maternal ewes bond quicker on subsequent
births, 209, 217
mother–infant recognition, 130–131, 218
no disassortative mating by MHC, feral sheep, 85
Ovulin, 89
(4Z,11Z)-Oxacyclotrideca-4,11-dien-2-one, 28
9-Oxo-2-decenoic acid (9-ODA), 215
Oxytocin, 78, 216–217, 218
Pachycondyla laevigata (ant)
mass recruitment, 150
Pachycondyla obscuricornis (ant)
individual hunter, 150
Panulirus interruptus (spiny lobster)
aggregation for defense, 105
Paraponera clavata (ant), eavesdropped by parasitoid fly, 246
Parcoblatta lata (cockroach)
monitoring as proxy for rare bird, 263
multicomponent sex pheromone, 28
Parkinson’s disease
sense of smell, loss, 283
Péclet number (Pe), definition, 228
Peg3, paternally imprinted gene, odor learning (mice), 209
Pella funesta (staphylinid beetle), uses propaganda, 255
Pentacosane, 155
Pentacosene, 155, 254
People. See Humans
Peptide pheromones, 30–31, 45, 72, 138, 213
Cynops spp. (newts)
species specificity, 25
darcin (mice), 124
exocrine gland-secreting peptide 1 (ESP1), 204–206
Rhitropanopeus harrisii (mud crab), pumping pheromone
(egg release), 110
Perfumes, 277, 281, 282
Periplaneta spp. (cockroach)
multicomponent pheromones, 28
Pesticides, resistance to, 266
Petromyzon marinus (sea lamprey)
larval (migratory) pheromone, 24, 267
pest management, 267
pheromone evolution, 21
sex pheromone, 267
3-keto petromyzonol sulphate, 22
tracking plumes, 241
Petromyzonol sulfate, 24
pgFAR fatty acyl reductase gene, 96
pH changes ligand interaction, danger from ocean
acidification, 46
Pharmacophagy, 31
Pheidole dentata (ant)
response to fire ant pheromone, 172
Pheidole oxyops (ant)
trail life, short, 158
Pheidole pallidulato (ant), recruits for heavy prey, 159
Phenol, 31
Phenolics, 246
Phenotypic matching, 130, 279
2-Phenoxyethanol, 23
Phenylacetonitrile, 271
Phenylethanol, 139
Pheromonal parsimony, 24–25, 43, 157
Pheromone biosynthesis-activating neuropeptide
(PBAN), 89
Pheromone-binding proteins (PBPs), 198
LUSH (OBP76a), 198
Pheromone-degrading enzymes in the sensillum lymph, 201
Pheromones. See also Aggregation; Alarm; Applications;
Bioassays; Costs; Glands; Apis mellifera; Host-
marking; Semiochemical identification; Primer effects;
Recruitment; Releaser effects; Scent marking; Signals
applications. See Applications of semiochemicals
aquatic, soluble polar, 167
brain wiring flipped in species using opposite ratios of same
molecules, 97
caste differences
production, 32
combinatorial processing in brain, 178–183
control of reproduction, 133–148
convergent, 24
costs of signaling. See Signals, costs
definition, 6
differences from signature mixtures, 9, 14
direct transfer, 23
into bloodstream, 30
evolution, 18–23
enabled by olfactory receptor proteins and combinatorial
brain circuits, 18
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from pre-existing chemical cues
alarm pheromones, 165
genomics approaches, social insects, 63
how demonstrate, 21–23
males responding to cues of previous mates, 22
match signal characteristics to requirements, function,
habitat, 23
receiver pre-adaptations (sensory bias model), 21
ritualization, 18, 19, 21, 113
salamander pheromones, 30–31
sender-precursor model, from cues, 18–21
evolutionary change in multicomponent pheromones, 31
excreted in urine, 19
glands
social insects, summarized, 135
gustatory response
invertebrates, 15
history, 5, 49
humans. See Humans
identification. See Semiochemical identification
induce gene expression in brain, 43, 62, 172
interaction with signature mixtures, 218–221
multicomponent
alarm
social insects, 170
challenges to identification, 54–55
social insects
trail, 157
solitary bees, 254
synergy, inevitable outcome of combinatorial
processing, 28
whole blend acts at a distance, 27, 95
neural processing (ON/OFF/AND) for YES/NO, 28
operational definition, 9–10, 23
primer effects. See Primer effects
production, 31–32
by microbes, 31
collect from plants, 31
synthesized by sender, 31
prompting learning other odors, 16
prompting learning, flexibility in behavior, 208–209
recruitment. See Recruitment pheromones
response, 43
conditional, 206
context dependent
aphids, 168
aphids tended by ants, 249
saltational shift, 29, 97
same molecules shared across species, 24
signals vs cues, 18
sources. See Pheromones, production
species share molecules if no selection against, 24
specificity
exploring chemical space for related molecules, 28
multicomponent, 28
unique molecule, 25–27
synergy, inevitable outcome of combinatorial
processing, 28
trail. See Recruitment pheromones
Philanthus triangulum (beewolf wasp)
males lek, 80
pre-existing female sensory bias for prey
pheromones, 21
Phodopus campbelli (Djungarian hamster)
recognition of individuals of other hamster species, 40
Phthorimaea operculella (potato tuber moth)
pheromone blend ratio varies with rearing temperature, 92
Picoides borealis (red-cockaded woodpecker)
monitoring cockroach prey by pheromone, 263
Pieris brassicae (large cabbage white butterfly)
anti-aphrodisiac, 88
eavesdropped, 245
Pieris napi (green-veined white butterfly)
anti-aphrodisiac, 88
Pieris rapae (small cabbage white butterfly)
anti-aphrodisiac, 88
Pigs. See Sus scrofa
Piperidine alkaloids, 212
Plankton, 230
larval settlement and metamorphosis, 110
Plants. See also Pheromones, production
“calling for help”, 244
feedstock precursors for synthetic semiochemicals, 273
orchids, pollination by sexual deception
aggressive chemical mimicry, 252–253
self-defense by producing herbivore alarm pheromone,
255
transgenics produce aphid alarm pheromone, 270
Platynereis dumerilii (polychaete worm)
pheromones co-ordinate external fertilization, 70, 110
Platysoma cylindrica (predatory beetle), eavesdropping, 246
Pleiotropy, 94
Plethodon shermani (red-legged salamander)
direct transfer of peptide pheromone to female’s nostrils,
23, 45
Plethodontid salamanders
pheromone evolution, 30–31
Plumes
eddy chemotaxis, 241
turbulence, visualization, 228, 235–238
Podisus maculiventris (spined soldier bug), eavesdropped by
parasitoid, 245
Poecilia reticulata (guppy, fish)
cryptic female choice, 89
Pogonomyrmex badius (harvester ant) alarm pheromone signal,
229
Pogonomyrmex barbatus (harvester ant)
CHCs of foragers recruit others, 160
Pogonomyrmex spp. (harvester ants), trail species
specificity, 157
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Polistes (paper wasps)
colony recognition, 129
evaded by cuckoo species, 257
Polistes dominulus (social wasp), 257
Polistes fuscatus (paper wasp)
kin recognition mechanisms, 129
visual recognition to distinguish individual colony
members, 40
Polistes metricus (paper wasp)
lacks specialized face learning abilities, 40
Polistes semenowi (social wasp, parasite), 257
Pollution, 45–46
anthropogenic carbon dioxide and ocean acidification
dangers to whole ecosystem by interference with
chemosensory systems, 46
endocrine-disrupting effects on olfaction, 45–46
pheromones in aquaculture, risk, 262
Polyergus rufescens (slave-making ant), use of propaganda, 255
Popilla japonica (Japanese beetle), 25
Pre-copulatory mate guarding. See Sperm competition
and mate guarding
Premnas spp. (anemonefish)
symbiotic with sea anemones, 249
Primates
chemical profile differences in related species, 91
Homo sapiens.See Humans
over-marking
female choice, 262
reproductive suppression, 146
rhesus monkeys
copulins, 299
scent marking, 124
manipulate mate choice, 262
Primer effects, 43–44, 300, See also Releaser effects
can be fast acting, 44
dauer pheromone (Caenorhabditis elegans (nematode)), 25,
210–211
intergenerational
alarm pheromones in aphids, 169
desert locusts, 106
mammals, 209–210
by either VNO or main olfactory system, 210
sexually dimorphic hypothalamic neurons releasing
kisspeptins, 200–201
menstrual synchrony, 300–301
modulation of hormone signaling and gene expression, 209
social insects
caste development, 211–213
transcriptomics, to investigate, 62
use in pest management, 271
Projection neurons, 183
Propaganda (use of alarm pheromones to manipulate other
species), 255
See also Deception
3-Propyl-1,2-dithiolane, 269
Prorhinotermes simplex (termite)
sex differences, 138
Prostaglandins, 45, 70
Prostephanus truncatus (larger grain borer beetle), 108
aggregation pheromone
monitoring, 263
males only signal until females arrive, 109
Proteles cristata (aardwolf), 123
neighbor recognition, 133
Protocerebrum, 183
Proust, smells bring back memories, 280
Pseudacanthotermes spiniger (termite)
trail and sex pheromones, same molecule at different
concentrations, 24
Pseudacteon tricuspis (phorid fly), eavesdrops host alarm
pheromone, 246
Pseudogates (termite nymphs), 138
Puberty acceleration. See Hormones
Puberty delay
rodents
questions about ecological relevance, 147
Public chemical information, 165
PUFAs (polyunsaturated fatty acids)
barnacle egg hatching pheromone, 110
Puntius (fish) (androgen effects on electro-olfactogram
(EOG)), 207
Purines, 107
Pyranones, 212
Pyrrolizidine alkaloids, 31
Quantitative trait locus (QTL), 29, 98, 103
Queen butterflies. See Danaus gilippus
Queen egg-marking pheromone, 36
Queen mandibular pheromone (QMP). See Apis mellifera
Queen pheromones. See also Ants; Apis mellifera; Pheromones;
Termites
as honest signal, 36, 214
developmental switches
mechanisms, 211–213
social insects, 137–146
Quorum sensing, 48
Rabbits. See Oryctolagus cuniculus
Racemic mixture (racemate), 307
Ram effect. See Male effect
Rattus norvegicus (Norway rat)
behavior manipulated by protozoan parasite Toxoplasma
gondii, 248
follows trails from good food sources, 155
sniffing in stereo, compare in olfactory cortex, 233
Receiver psychology (hidden preferences), 21
Recognition, 215–218
dominants, reproductive suppression, 146
imprinting, 38–40
learning, 38–41
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mammals, 130–133
clan or group, 131–132
individual recognition, 132–133
kin, 131
mother–offspring, 130–131
prairie vole partners, mechanisms, 218
some glands more variable than others, 133
mechanisms, 37
bioassays to study, 52
greenbeards, 40
individual recognition, challenges in demonstrating,
132–133
phenotypic matching, 38, 130, 131, 279
self-matching (armpit effect), 38
template, 13
mothers and babies, 278–279
social insects
colony and kin recognition, 126–130
learning needed before discrimination, 126–130
social species
have more complex chemical profiles?, 41–42
template, 13
brain imaging, social insects, 216
Recruitment pheromones. See also Alarm pheromones;
Self-organizing systems
alarm (social insects), 169–172
Apis cerana japonica (Japanese honeybee), 170–171
coordinate defense, 170–171, 255
marking enemies for further attack, 169,
170, 171
termites, 171
ants
alarm, 170
competition strategy, 157
group recruitment, 153
mass communication, 153
modeling foraging, 160–161, 162
multiple pheromones, flexibility, 159
tandem running, 153
trail components with different roles, 50
trail specificity, 157
bumblebees
foraging recruitment pheromone, 155
colony specificity
stingless bees, 155
expand colony diet, 153
food distribution, recruitment type, 150–153
Heterocephalus glaber (naked mole rat)
recruitment of foragers, 155
honeybee
with waggle dance, 155
longevity related to food supply, 158
Malacosoma americanum (tent caterpillar), 152
matching foraging effort to food value, 159–160
Rattus norvegicus (Norway rat) follow trails from good food
sources, 155
social insects to co-ordinate attack, 169
species specificity
ants, 157
stingless bees, 155
termites, 155–157
stingless bees (Meliponini)
odor beacons, 154–155
termites
foraging patterns, 158
Trigona spp. (stingless bees)
odor beacons, 156
Redundancy (signal), 54
Reinforcement (selection against hybridization), 90
Releaser effects, 43–44, See also Primer effects
Reliable signals. See Signals, honest
without handicap
individual or colony identity, 36
Replication
common lack of, 53
good example of value, 210
vs. quasireplication, 53
Reproductive skew, 136, 137
Reproductive suppression
primates, 146
Reticulitermes santonensis (termite)
sex differences, 138
Reticulitermies flavipes (termite)
host to beetles, 257
soldier terpenes change workers’gene expression, 212
Reticulitermies speratus (termite)
queen pheromones and caste development, 139, 212
Reynolds number (Re)
copepod pheromone trails, 230
definition, 228
effects on sense organ design, 184
Rhagolitis pomonella (apple maggot fly)
learning own scent marks, 209
Rhinella marina (cane toad)
alarm cue, 269
management of, 269
Rhitropanopeus harrisii (mud crab)
pumping pheromone (egg release), 110
Ritualization, 18, 21
RNA interference (RNAi), 60, 213
RNA-seq, 62–63, 91
Ropalidia marginata (paper wasp)
colony recognition mechanisms, 129
non-kin may join colony, 129
Rotifers
do not use diffusable pheromones, 227, 230
sex pheromones, 60
Royal jelly (honeybee), 213
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Royalactin (honeybee), 213
Runaway sexual selection, 74
Saccopteryx bilineata (greater sac-winged bat)
semiochemicals, microbial contribution, 41
Saguinus fuscicollis (saddle-back tamarin)
chemical profile, multiple messages in odors, 126
Salaria pavo (peacock blenny, fish)
male parental care, 77
honest signal, 35
Saltational shifts, 29, 97
Satellite males. See Alternative mating stategies
Saturnia pyri (great peacock moth)
Farbre’s early account, 5
Scale, 229
communication strategies, 227, 230
diffusable pheromones in water, 229
sensory organs, functional design, 185
Scaptotrigona postica (stingless bee), odor beacon
recruitment, 157
Scent marking, 118
advertises dominance and/or reproductive status, 114, 115,
124
captive breeding, exploiting scent marks, 262
conspicuous signals, 123
ecological factors and marking patterns, 115, 121, 123
males directly mark females, 124
marking rates, dominants and subordinates, 118
non-territorial mammals, 124
pest management
predator odors, as deterrents, 269
response varies by competitive ability, 118, 115, 118
scent-fence hypothesis, 115
scent-matching hypothesis, 115–118
reducing cost of territorial defense, 116
self-marking and presentation, 115
use to manipulate behavior, 262
using to census, 263–264
using vertebrate scent marks to manipulate behavior, 269
Schedorhinotermes lamanianus (termite)
foraging, 158, 159
Schistocerca gregaria (desert locust)
adult cohesion pheromone, phenylacetonitrile, 271
aggregation pheromones, 106
gregarizing factor on eggs, 106
intergenerational effects, 106
oviposition pheromones, 106
possible control of gregarization, 271
solitarious gregarious phases, 106
Schistosoma mansoni (nematode)
sex pheromone, 266
Schreckstoff, 166, See Alarm cues, fish
Scramble competition, 69–71
moth males, 69
selection on male moths, 70
Sehirus cinctus (subsocial bug)
solicitation pheromone, begging, 36
Self-organizing systems, 160–163
ant foraging, 160–161
stochastic effects, 161
stigmergy, 162
termite nests, 161–163
Self-referent (“armpit”) matching, 38
Semibalanus balanoides (barnacle)
egg hatching pheromone
eicosanoids (PUFAs), 110
Seminal fluid molecules
allohormone pheromones, 88–89
behavioral manipulation, 45
prostaglandins, 45
Semiochemical identification
bioassays. See Bioassays
collection and analysis, 55–59
activity-led fractionation, 56–57
gas chromatography–mass spectroscopy (GC–MS), 57
high performance liquid chromatography (HPLC), 55
liquid-chromatography–MS (LC–MS), 57
nuclear magnetic resonance spectrometry, 57
collection and analysis without fractionation, 57–58
headspace sampling, 57
in situ analysis, 57
metabolomics, 57–58
near-infrared spectroscopy (NIRS), 57
nuclear magnetic resonance (NMR) spectrometry, 58
solid-phase microextraction (SPME), 57
stir-bar sorptive extraction (SBSE), 57
UV laser desorption/ionization orthogonal time-of-flight
MS (UV–LDI–TOF MS), 57
loss-of-function mutants as tool, 50, 58
molecular biology and genetics as tools, 59–63
cautions, misleading effects, 60
gene manipulations, 60–62
genomics, 62–63
knockouts, transgenics, 60
morpholino oligonucleotides, 60
optogenetics, 60
RNA interference (RNAi), 60
RNA-seq, 63
visualizing neural circuits, 60–62
no single ideal approach, 58
pheromones (operational definition), 9–10
Semiochemicals. See also Bioassays
applications. See Applications of semiochemicals
cues
definition, 18
definitions, 1, 6
allelochemicals, 1
allomones, 1
chemical profile, 2
kairomones, 1
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pheromones, 5
pheromones (operational definition), 9–10
signature mixtures, 10
synomones, 1
innate, 16
signature mixtures and pheromones compared, 9, 14
Sensitive periods, 216
behavioral development, 16
imprinting, 16
learning colony odors (social insects), 129
Sensory bias
food molecules, 21
host-plant odors, 21, 99
pre-existing sensitivities exploited by signalers, 21
prey pheromones, 21
Sensory organs
functional design, 185
Sensory trap
contribution to pheromone evolution, 21
Septal organ of Masera, 195
Serotonin (5-hydroxytryptamine) (5HT), 208
Settlement inducing protein complex (SIPC), 109
Sex-specific neural circuits
insects, 201–204
moths, 201
mammals, 204–206
Sexual conflict, 31
anti-aphrodisiac pheromones, 87–88
costs of “sensory trap”,21
driving sex peptide variety, 21, 89
interference in partner’s signaling to prevent
competitors, 69
seminal fluid molecules, 88–89
Sexual dimorphism
hypothalamus, kisspeptin neurons, 200–201
moths, male antennae and brain, 201
Sexual selection
conflict between the sexes, 69, 87–88, 89
contests, 72–73
co-ordination, external fertilization, 69
definitions, 65–66
forms of, 65
mate choice, 73–87
mechanisms
indicators, 74
overview, 73–75
post-copulatory, 87–90
anti-aphrodisiacs, 87–88
cryptic choice of sperm by female, 89–90
based on MHC, 85
seminal fluids, 88–89
sperm competition, 89
pre-copulatory mate guarding, 71–72
scramble competition, 69–71
species-specific secretory glands, 66
variety of pheromone glands in males, 31
which sex should advertise, 66–69
Sharks
lateral line for rheotaxis, 241
plume tracking, 226
Sheep. See Ovis aries
She-males. See Alternative mating strategies
Signals. See also Pheromones
communication, 18
costs
acoustic signals (high metabolic cost), 34
efficacy cost, 32, 34
energy as proxy for fitness costs, 34
pheromones
most, low costs, 34
some, high efficacy costs (time, energy, risk), 34–35
risk investigating marks, beavers, 114
strategic cost (handicap cost), 32
time marking, antelope, 114
cues vs. signals, 18
definition, 18
duration, 23
extending signal life, 23
evolution
co-evolution of sender-receiver, 30–31
match signal characteristics to requirements, function,
habitat, 23
receiver psychology (hidden preferences), 21
handicap theory, 32, 33–34
honest (reliable) signals without handicap, 32–37
body condition and testosterone/androgen effects on males,
75–76
indices (unfakeable signals), 35–36
other costs including predation, 37
shared interest including kin selection, 36
signs of paternal investment, poisons and parental care,
76–77
social cost (punishment), 36–37
social insect queen pheromones, 137–146
how receivers follow changes in signal, 93–94
minimal cost signals, 32–37
multimodal signals, 44–45, 75, 167, 171
challenge for bioassays, 54
pheromone and tactile signals, 150
scent marks with ultraviolet cue, 123
sound and odors, 155, 157
queen pheromones
control or co-operative signal, 137–146
redundancy, 44, 54, 167
challenge for pheromone identification, 54
deer alert signal, 44
ritualization, 21
Signature mixtures, 10–15, 278, 280
as “receiver-side”phenomenon, 2, 15
definition, 6, 10
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Signature mixtures (cont.)
differences from pheromones, 9, 14, 37
identification. See Bioassays
interaction with pheromones, 218–221
learning, 37, 38–41, 215–218
olfactory system, 37
social insect variation in trail marking between colonies,
stingless bees, 155
social mammals
individual recognition and reproductive suppression,
146–147, 219
Simulidae (blackfly)
oviposition pheromones, 106
Single nucleotide polymorphisms (SNPs), 191, 294
olfactory receptors, 292
secretions (ABCC11), 290–291
Sitophilus (stored product beetle), 108
Smell. See Olfaction
Smell-O-Vision, 303
Snakes
anti-aphrodisiac pheromones, 88
Coolidge effect, 86
show defensive behavior to predatory snake odors, 248
trail following
forked tongues, role, 232
tropotaxis, 232
Sniffing
in stereo, 233
initiates oscillations in brain, 186, 187
SNPs. See Single nucleotide polymorphisms
Social insects. See also Ants; Eusociality; Apis mellifera;
Recruitment pheromones; Self-organising systems;
Termites
alarm pheromones, 169–172
evolved from defensive molecules, 20–21
caste development, 211–213
caste differences
pheromone secretions, 32, 135
response to pheromones, 135
colony and kin recognition, 126–130
colony level selection, 214
colony odors, 36, 134
selection by parasites for greater diversity in hosts, 42
selection by social parasites for greater diversity inhosts, 258
sources, 41
communication largely minimal-cost, kin selection, 36
co-opting genes from solitary ancestors, 215
differences between queens and workers
gene expression, 214
fertility signal, 36, 137–146
genetic CHC differences between patrilines, 130
guards
defense of colonies, 126, 170
importance of colony defense, 170
individual recognition by founding ant queens, 38
key roles for pheromones, enabling sociality, 134
main pheromone glands, summarized, 135
multicomponent pheromones, 28
multiple uses of the same pheromone (pheromone parsimony),
135
newly eclosed, need to pick up colony odor, 129, 130
parallels with social mammals, 147–148
queen egg-marking pheromone, 36
queen pheromones
control or co-operative signal, 137–146
genomics to explore evolution of, 63
reproductive conflict, 136–137
suicidal defense, 169, 170, 171
territories, 116
worker policing, 36, 142–146
workers on different tasks
differences in brain gene expression, 214
Social mammals. See also Eusociality
clan recognition, 132
ecological factors, 147
parallels with social insects, 147–148
reproductive conflict, 136–137
reproductive control
not by pheromones, 146–147, 219
suppression of helper reproduction, not by pheromone,
146–147, 219
Sociogenomics, 212
Solanum berthaultii (wild potato), produces aphid alarm
pheromone, 255
Solenopsis invicta (fire ant)
alarm pheromones eavesdropped by phorid fly, 246
enemy specification, 172
greenbeard gene Gp-9,40
mass communication, 153
queen mutual inhibition, 212
queen pheromones, 212
queen pheromones, as control, 271
recruitment, 159
trail pheromone, 231, 270
alerting and orienting components, 50
Solid-phase microextraction (SPME), 57
Speciation, 24
allopatric, 90
assortative mating (like with like), 90, 96
asymmetric tracking, 94
disruptive selection, 94
ecological races, 92
infertile hybrids, 91
mate choice, 31
pheromones allow rare morphs to find each other, 94
pre-mating isolation, role for chemosensory barriers, 91
process
signal change, how receivers track changes, 93–94
reproductive character displacement, 90
selection against hybridization (reinforcement), 90
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Index
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Tristram D. Wyatt
Index
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www.cambridge.org© in this web service Cambridge University Press
sexual selection
role in founding phase of new island
populations, 92
signal change, few genes involved, 278
signal changes involving many genes,
polygenic, 29, 97–98
signal variation, within and between populations, that
selection can act on, 92–93
sympatric, 90
orchids, different pollinators, 253
Speciation genes, 91, 101
Sperm competition, 89
Spermophilus beldingi (Belding’s ground squirrel)
kin recognition cues, 131
Spiders
conflict between the sexes, 69
Spodoptera littoralis (moth)
bat clicks increase male response to
pheromone, 44
Sry gene, sexual differentation in mammal
embryo, 206
Stabilizing selection, 92, 93
Standing behavior. See Lordosis
Staphylococci, 288
Stereoisomers (spatial isomers), 25, 306
Stigmergy, 162
Stingless bees (Meliponini)
robber species and resistance, 255
trail beacons to food sources, 154–155
Stir-bar sorptive extraction (SBSE), 57
Stomatopod
antennal flicking rate scales with increasing size in
lifetime, 186
Stored product insects
monitoring, 263
Stored-product beetles, 108
Strategic cost, 32
Subesophageal ganglion (SEG). See Suboesophageal
ganglion (SOG)
Suboesophageal ganglion (SOG) (insects)
gustatory sensory neurons (GSNs), feed to, 197
Sulfanylalkanols (thio-alcohols), 290
Sulfated amino-sterol, 72, 79
Sulfated steroids, 195
Supella longipalpa (brown-banded cockroach)
unique molecule as sex pheromone, 25
Supellapyrone, 25
Superparasitism
host marking, to avoid, 110
Sus scrofa (pig)
advancing puberty, 261
Boarmate
TM
lordosis readiness test for AI, 261
reduces aggression, young pigs, 263
reduces postpartum interval, 261
Sweatbees
colony recognition, 128–129
Synergy, 58, 142
definition, 28
natural outcome of combinatorial processing, 28
testing, 28
Talpa europaea (mole), territories, 115
Taste
compared with smell (olfaction), 175
smell (olfaction) vs. taste (gustation), 15, 173
Taxis, 224, 225
Telenomus euproctidis (parasitoid wasp), phoresy, 245
Teleogryllus oceanicus (cricket)
male adjusts ejaculate vs. sperm competition, 89
uses CHC profiles to avoid genetically similar mates, 81
Teleology, 223
Temnochila chlorodia (predatory beetle), 246
Template (for recognition), 15, 127
brain imaging, social insects, 216
definition, 13
Termites
alarm pheromones, 169–172
caste-change pheromones, 212
colony recognition, 130
differences from Hymenoptera, 138
differences in gene expression, queens vs. kings and
workers, 139
nest building as self-organizing system, 161–163
pheromonal parsimony, 24, 157
pheromones and foraging patterns, 158
primer effects, 138–139, 212
queen pheromones, 212
sex differences in signals
polar proteinaceous secretions, 138
soldiers, control of numbers, 139, 212
suicidal defense, 171
trail following, 232
trail pheromones, 155–157
used as sex pheromones, at high concentration, 157
Territories, 113, 116, See also Scent marking
“owner advantage”, 116
dear-enemies, 118, 123
economics of scent marking, 121–123
hinterland and perimeter marking, 121, 123
variation by habitat, 121, 123
group defense, 113, 114, 120–121
nasty neighbors, 123
scent marking, 118
border maintenance hypothesis, 120–121
composite signals with ultraviolet cue, 123
lamp-post effect, 44, 123
scent fence hypothesis, 115
scent matching hypothesis, 115–120
social insects, 116
Index
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403
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Tristram D. Wyatt
Index
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Testosterone. See Hormones
Tetanolita mynesalis (moth)
victim of bolas spider, 251
(E)-11-Tetradecenyl acetate, 29, 96
(Z)-9-Tetradecenyl acetate, 251
(Z)-11-Tetradecenyl acetate, 29, 95, 96
(Z,E)-9,12-Tetradecenyl acetate, 251
Tetradecyl acetate, 255
Tetragonisca angustula (stingless bee)
alarm pheromones to activate colony defense, 255
resists raids by robber bees, 255
Tetramorium caespitum (ant), foraging, 161
Thamnophis sirtalis parietalis (red-sided garter snake)
anti-aphrodisiac, 88
chooses mates from own population, 84
males choose females in better condition, pheromone
based, 76
population differences in chemical profiles, 92
semen effects on female behavior, 45
she-males, 87
trails
detecting direction, 233
following, 232
Thanasimus dubius, (predatory beetle),
eavesdropping, 246
Thiazole. See Butyl dihydrothiazole
Ticks
aggregate on scent marks of mammal hosts, 246
assembly pheromone
ecophysiological benefits, 107
guanine, assembly pheromone, 107
pheromones, to control, 266
Tiger moths. See under Utethesia ornatrix
Tomicobia tibialis (parasitoid wasp), eavesdrops bark beetle
host, 247
Tools to study pheromones. See Bioassays; Semiochemical
identification
Toxoplasma gondii (protozoan parasite)
changes rat’s fear of cat odor to attraction, 248
Trace amine-associated receptors (TAARs), 192, 193
Trade-offs, of energy allocation, 35
Trail pheromones. See Recruitment pheromones
Transcriptome, 62
Transforming growth factor-β(TGF-β) peptides, 211
Tribolium castaneum (flour beetle)
aggregation pheromone, 109
cryptic female choice, 89
Trichogramma brassicae (parasitoid wasp),
phoresy, 245
Trichogramma evanescens (generalist parasitoid), learns host
pheromones, 245
Trichogramma pretiosum (parasitoid wasp), oviposition
marking, 110
Trichoplusia ni (cabbage looper moth)
both sexes call, 69
Trichoplusia ni (cabbage moth)
multicomponent pheromone
redundancy, 54
pheromone blend shift, males follow, 30, 96
Trichopsenius frosti (beetle), matches its termite host, 257
Tricosane, 155
Tricosene, 254
Z-(9)-Tricosene, 155
(E)-4-Tridecenyl acetate, 266
Trigeminal system, 195
Trigona spp. (stingless bees), 154–155, 255
odor beacon recruitment
Trigona corvina, 155
Trigona hyalinata, 157
Trigona recursa, 154, 156
Trigona spinipes, 154
victim to propaganda pheromones
Trigona subterranea, 255
Trimethyl-thiazoline, 187
Tritrophic systems, 244
Trogoderma glabrum (khapra beetle)
aggregation pheromone, 109
Trophallaxis, 129, 138
TRP2C, 199
Ultraviolet (UV) cues
Dipsosaurus dorsalis (desert iguana), multimodal signal with
UV, 44
Ultraviolet laser desorption/ionization orthogonal time-of-flight
mass spectrometry (UV–LDI–TOF MS), 57
Unintended bias in experiments, avoiding, 53
Uric acid, 70
Uridine diphosphate, 71
Utetheisa ornatrix (tiger moth)
cryptic female choice, 90
female choice, 76
honest signal, 35, 76
hydroxydanaidal (HD) from diet, 31, 76
male pheromone evolved by sensory
exploitation, 99
cis-Vaccenyl acetate (cVA) 62, 253
Vandenbergh effect, 210
Vanillic acid, 266
Varroa destructor (parasitic mite)
response to honeybee larval odors, use as
kairomones, 136
Vasopressin, 218
Vertebrate pests
Castor canadensis (beaver), 269
Cyprinus carpio (common carp), 267
Mustela vison (American mink), 263
Petromyzon marinus (sea lamprey), 267
Rhinella marina (cane toad), 269
scent marks to census, 263–264
404
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Index
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978-0-521-11290-1 - Pheromones and Animal Behavior: Chemical Signals and Signatures: Second Edition
Tristram D. Wyatt
Index
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Verticillium lecanii (fungal pathogen), 270
Vespa mandarinia japonica (giant hornet), 170–171
Vespula germanica (wasp)
eavesdropping prey leks, 37, 245
Vespula vulgaris (wasp)
marks with sting venom, alarm, 171
Vipera berus (adder, snake), Coolidge effect, 86
Vitellogenin, 214
Vomeronasal olfactory system
memory and pregnancy block (Bruce effect), 219–221
molecular architecture and differences from main
olfactory system (MOE), mapping to glomeruli,
receptor proteins, 193–195
Vomeronasal organ (VNO), 193–195
humans, vestigial, 291
Vomeronasal receptors VRs, 193–195
Westermarck or kibbutz effect
human mate choice, 279
Whales and dolphins, 12
Whitten effect, 146, 210, 220
Wikipedia, how scientists can contribute, xiv
Worker policing, 36, 142–146
Xiphophorus spp. (swordtails, fish), leads to sexual isolation of
two species, 75
Xylotrechus pyrrhoderus (beetle)
stereochemistry of pheromone, 309
Yponomeuta ssp. (small ermine moths)
sympatric, avoiding cross-attraction
calling time, host plants, pheromone blend, 95
Zigzag, tracking trail or plumes, 236
albatross, 242
dogs, 233
humans, 233
moths, 240
snakes, 233
Zootermopsis nevadensis (termite)
fertility signaling, 138
laying trail, 154
Index
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405
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978-0-521-11290-1 - Pheromones and Animal Behavior: Chemical Signals and Signatures: Second Edition
Tristram D. Wyatt
Index
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