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Sexual selection and reproductive competition in primates: New perspectives and directions

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Book Reviews
Physiology of the Graafian Follicle and
Ovulation. R.H.F. Hunter. x + 378 pp.
Cambridge, UK: Cambridge University
Press. 2003. $90.00 (cloth).
Physiology of the Graafian Follicle and
Ovulation is a superb review of more than
100 years of descriptive, experimental, and
clinical literature that spans neuroendo-
crinological, immunological, histological, and
genetic aspects of follicular development and
ovulation. Throughout the monograph, R.H.F.
Hunter communicates his long-standing enthu-
siasm for understanding the ovarian process-
es central to reproduction. Along the way, he
reflects on the tension between ‘computer-
based living’ and the simplicity of paper and
pen, as well as between molecular biologists
and practitioners of descriptive biology. Al-
though his preferences are paper, pen, and
description, Hunter is obviously well-versed
in other methods and points of view. He details
and synthesizes differing opinions, addresses
confusions in the literature that result from
different techniques, and integrates research
findings across a variety of species.
Hunter grapples with fascinating ques-
tions, such as why primordial germ cells mi-
grate to the genital tissues during embryo-
nic development, why Graafian follicles grow
so large, and how meiosis is triggered to
resume at the leutenizing hormone (LH)
surge. He offers a wealth of detail on such
topics as ovarian blood flow, ovarian tempera-
ture gradients, potential clinical markers of
follicle reserves (inhibin B) or oocyte quality
(acivin A), and the potential role of granulosa
cells released with the oocyte at ovulation.
The book is beautifully crafted, with careful
transitions and a linear development of ideas
across chapters. Some points are repeated
(e.g., the reflux of follicular fluid from the
Fallopian tube and how the preovulatory fol-
licle functions as a corpus luteum following
the gonadotrophin surge), but the perspective
shifts each time and the repetition seems
appropriate. The final chapter (Chapter XII)
provides a summary of high points.
Chapter I reviews historical landmarks in
the study of mammalian ovaries, Graafian
follicles, Fallopian tubes, and oocytes. The
review extends from classical antiquity to the
current century. For example, while de Graaf
‘fully appreciated the problem of dimen-
sions of the ovarian follicles in relation to the
diameter of the Fallopian tubes (p. 11), it was
von Baer who finally dispelled the confusion
between eggs and follicles in 1827.
Chapter II addresses the formation and
structure of ovaries, from the gene pathway
by which an ovary differentiates to the migra-
tion of primordial germ cells. Genetics and
descriptive biology are integrated to describe
the development of oocytes and, later, the
development of follicles. Chapter III focuses
on the physiology of ovaries, including vas-
culature, lymphatic pathways, and ovarian
innervation. Hunter is particularly interested
in the role of the autonomic nervous system in
ovarian function. Later on, the discussion of
the temperature gradient within the pre-
ovulatory follicle is fascinating. According to
Hunter’s review, the antral fluid temperature
of human follicles can be as much as 2.3C
cooler than ovarian stroma, a difference that
may reduce the frequency of mutation in
maturing germ cells or benefit the cytoplas-
mic maturation of oocytes (p. 95).
Chapter IV details ovarian follicular fluid.
Of particular interest is the suggestion that
follicular fluid evolved ‘‘to play a crucial role
in follicle selection and dominance (in contrast
to a massive unselected wave of ovulation in
aquatic ancestral species)’ (p. 131). Chapter V
surveys estradiol synthesis by the Graafian
follicle and describes the role of ovarian pro-
teins—inhibin, activin, and follistatin—as
well as peptide growth factors, endorphins,
enkephalins, and nitric oxide. In addition, con-
tributions of the immune system to the regu-
lation of cyclic ovarian activity are detailed.
Chapter VI provides an overview of folli-
cular recruitment, selection, dominance, and
atresia. Interesting problems include how the
dominant follicle inhibits follicular matu-
ration in the contralateral ovary and the
relative contributions of the processes of
necrosis and apoptosis to the loss of oocytes.
Chapter VII reviews the preovulatory surge
of gonadotrophic hormones, evidence for an
ovarian gonadotrophin surge inhibiting or
attenuating factor (GnSAF), and how the
extracellular matrix and basement mem-
brane must be continuously remodeled due
to the constantly changing nature of the folli-
cle population.
Chapter VII addresses the process of
ovulation—the event to which the preceding
chapters have been building. As Hunter de-
monstrates, the process of ovulation (spon-
taneous and induced) is a fascinating topic of
ß2004 Wiley-Liss, Inc.
AMERICAN JOURNAL OF HUMAN BIOLOGY 16:172–178 (2004)
research ‘in part because successful release
of a potentially fertilizable egg from the
ovary into the Fallopian tube is such a vital
event’ (p. 268). It is also ‘a multi-factor-
ial, multi-compartmental event’ with ‘a be-
wildering array of molecules to consider’
(p. 284).
Chapter IX discusses the postovulatory cor-
pus luteum, the Fallopian tube (another tem-
perature gradient!), follicular fluid, and the
role of cumulus cells liberated along with the
oocyte from the follicle. Because follicle cells
remain in fluid suspension in the vicinity of
the oocyte or newly fertilized egg, Hunter
argues, they may play a supportive role as a
paracrine tissue.
Chapters X and XI are clinical in empha-
sis, although Hunter takes a physiological
approach. Chapter X provides a discussion of
clinical conditions that result in a failure of
ovulation, e.g., Turner’s syndrome. Chapter
XI addresses the induction of ovulation in
women and domestic animals.
Hunter’s writing is very clear, but he pre-
sumes a significant degree of prior knowledge
about anatomy, endocrinology, immunology,
and genetics. The illustrations have been
carefully selected. Physiology of the Graafian
Follicle and Ovulation is basic science at its
best, with implications for the treatment of
infertility, the evolution of menopause, and
an understanding of variation in age at meno-
pause.
Although the Preface states that this could
be a useful text for advanced undergraduates,
as well as medical and veterinary students,
Hunter hints later that the perceived audi-
ence for his text includes medical colleagues
who may not know about observations made
in veterinary clinical departments, and over-
worked university lecturers who lack time to
devote to laboratory work or extensive read-
ing. For human biologists, the text serves as
an excellent reference for the particulars of
ovarian physiology; however, it is too specific
and detailed to be assigned in a class on repro-
ductive ecology. Although there are mentions
of the effect of seasonality, nutrition, and/or
stress on IGF-I (p. 160), the extent of apopto-
sis (p. 212), the lifespan of an oocyte (p. 314),
and ovulation failure (p. 336–7), the ideas are
not developed. That being said, Physiology of
the Graafian Follicle and Ovulation is a won-
derful reference for teachers of growth and
development (Chapter II in particular) and
reproductive ecology. It is an essential book
for biological and medical libraries and for
anyone interested in the physiology of repro-
duction.
LYNNETTE LEIDY SIEVERT
Department of Anthropology
University of Massachusetts
Amherst, Massachusetts
DOI: 10.1002/ajhb.20004
Rethinking Homeostasis: Allostatic Regula-
tion in Physiology and Pathophysiology.
By Jay Schulkin. xviii +296 pp. Cam-
bridge, MA: MIT Press (A Bradford Book).
2003. $50 (cloth).
Most of us who were taught physiology
courses are familiar with general concepts of
homeostasis, adaptation and stress. Living
organisms have developed an array of mechan-
isms to maintain internal constancy in the face
of external challenges. However, applying
these terms to realities of life can be proble-
matic. In his recent bestseller, ‘Jarhead,’’
describing a U.S. Marine’s experience in the
Gulf War, A. Swafford (2003) shows a scene
where the Marines anticipating their deploy-
ment to the frontlines binge on Vietnam War
movies and alcohol. This scene is very emo-
tional: hyping themselves up for violence
these soldiers are in a state of fear. In this
state they show different strategies to cope
with their condition: ‘violent indifference,
fake ease, standard-issue bravura.’ However,
the condition of these Marines is impossible
to describe in all familiar physiological terms.
The soldiers do not yet experience the stress
of violence, so there is no need yet for adapta-
tion to this stress. The behavior of these indi-
viduals is anticipatory to the violence, and
clearly their physiological systems are not
working in a homeostatic fashion to bring the
internal state to the initial constant level. In
other words, homeostasis, adaptation, and
stress can only go so far in explaining a system
trying to maintain equilibrium in response to
external stressors, while examples from life
illustrate that organisms often undergo antici-
patory long-term changes in state.
In Rethinking Homeostasis, Jay Schulkin
provides a serious analysis of the concept of
allostasis and its usefulness to explain the phy-
siology of such changed conditions. Allostasis,
a term much less familiar than homeostasis,
was introduced by P. Sterling and J. Eyer
(1988), and refers to a change in body state
BOOK REVIEWS 173
in order to achieve viability. The term became
more popular after B.S. McEwen and col-
leagues (e.g., McEwen and Stellar, 1993;
McEwen, 1998) started to distinguish allosta-
sis (as a changed state of the organisms experi-
encing or anticipating stress) from allostatic
load (as pathophysiological consequences of
extended allostasis). Schulkin et al. (1994)
were among the first authors to address the
concepts of allostasis and allostatic load in
their research. These concepts are slowly
becoming more popular, especially through
the popular books on stress by McEwen
(2003) and R.M. Sapolsky (1998), but their
use outside of the stress physiology field is
sparse (with the important exception of the
introduction of an allostatic state in the drug
abuse literature by G.F. Koob and M. LeMoal
[2001]). Rethinking Homeostasis, therefore, is
very valuable in its attempt to show the broad
application of the concept of allostasis.
The first chapter of the book provides an
excellent historic perspective on this term
and its relation to the previously used
concepts, including homeostasis, heterosta-
sis, stress, predictive homeostasis, reactive
homeostasis, and rheostasis. It also intro-
duces the reader to the importance of feed-
forward positive regulation in allostasis. The
second chapter shows the usefulness of feed-
forward neuroendocrine systems to explain
motivation and central motive states. The
third chapter then explains in detail the
most classical example of allostasis: the role
of corticotropin releasing factor (CRF) in the
anticipatory extra-hypothalamic regulation
of fear, and its interaction with the hypo-
thalamic-pituitary-adrenal (HPA) axis. This
chapter also discusses the relation of this
regulation to inhibited children, unipolar
depression, and posttraumatic stress disor-
der. In chapters 4 and 5, less known exam-
ples of allostatic regulation are discussed:
normal and pathological facilitation of par-
turition and development of alcohol and
drug addiction. The book concludes with a
synthesis of the described chapters, high-
lighting the usefulness of the concept.
Overall, this book summarizes an impress-
ive amount of results from large and diverse
areas of research. It demonstrates clearly that
trying to explain physiology and behavior of
complex organisms is impossible in the old
terms of homeostasis and stress-response.
Teaching allostasis should be considered
along with classical homeostasis in physiology
and systems neuroscience courses. This book
could serve as an excellent source of refer-
ences for such a course. The book is well illu-
strated, although at times I felt that the figure
legends could be more detailed. The book
could be difficult for an unprepared student,
as it does not provide the details on basic and
specific mechanisms of the HPA axis (for
example, existence of alternative ligands of
CRF receptors and the CRF-binding protein
are not explained). The reader of this book
should come prepared with basic knowledge
of HPA axis and peptide regulation. However,
this book will be very useful as a source of
reference and examples for teachers updating
their courses to include modern concepts in
physiology, or for prepared researchers inves-
tigating allostatic effects in their system of
interest. Taken together, this book provides
one of the deepest looks into the concepts of
allostasis in the recent literature.
LITERATURE CITED
Koob GF, LeMoal M. 2001. Drug addiction, dysregula-
tion of reward, and allostasis. Neuropsychopharma-
cology 24:94–129.
McEwen BS. 1998. Stress, adaptation, and disease: allos-
tasis and allostatic load. Ann NY Acad Sci 840:33–44.
McEwen BS. 2003. End of stress as we know it.
Washington, DC: DANA Press, Joseph Henry Press.
McEwen BS, Stellar E. 1993. Stress and the individual:
mechanisms leading to disease. Arch Intern Med
153:2093–3101.
Sapolsky RM. 1998. Why zebras don’t get ulcers: an
updated guide to stress, stress-related diseases, and
coping. New York: W.H. Freeman.
Schulkin J, McEwen BS, Gold PW. 1994. Allostasis,
amygdala, and anticipatory angst. Neurosci Biobehav
Rev 18:385–396.
Sterling P, Eyer J. 1988. Allostasis: a new paradigm to
explain arousal and pathology. In: Fisher S, Reason J,
editors. Handbook of life stress, cognition, and health.
New York: John Wiley & Sons. p 629–649.
Swafford A. 2003. Jarhead. New York: Scribner.
ANDREY E. RYABININ
Department of Behavioral Neuroscience
Oregon Health & Science University
Portland, Oregon
DOI: 10.1002/ajhb.20008
Microarrays for an Integrative Genomics.By
Isaac S. Kohane, Alvin T. Kho, and Atul J.
Butte. xx + 306 pp. Cambridge, MA: The
MIT Press (A Bradford Book). 2003.
$40.00 (Cloth).
Life depends on the transcription of genes
into RNA. Accordingly, a major focus in bio-
logical research is the systematic identification
174 BOOK REVIEWS
of all genes that either are or are not expressed
in health and disease. Such studies have tradi-
tionally been slow and laborious and have
focused on one gene at a time. The recent
advent of DNA microarray technology for the
comprehensive analysis of RNA expression
(expression profiling), however, has revolutio-
nized experimental biology. Microarray experi-
ments can not only delineate the relative
expression of single genes, but also can reveal
patterns of gene expression, thus offering glo-
bal overviews of genetic activity that can be
quite informative about biological states.
DNA microarray-based gene expression pro-
filing relies on nucleic acid hybridization and
the use of nucleic acid polymers, immobilized
on a solid surface, as probes for complemen-
tary gene sequences. They are relatively easy
to use and can be applied to large numbers
of samples in parallel, allowing for the simul-
taneous measurement of expression across
theentiregenomeandmultisamplecom-
parisons. Advances in microarray technology
or design and decreasing costs are making
affordable, commercially available whole gen-
ome arrays commonplace. The major chal-
lenges now are the effective application of
these tools to biological questions and the sta-
tistically principled analysis of datasets that
can contain millions of measurements.
As with other front-line technologies, the
prospect of performing a DNA microarray
study can be daunting for the uninitiated.
These studies are multidisciplinary in nature,
requiring in-depth knowledge in molecular
biology, computational biology, and statistics.
Luckily, Kohane, Kho, and Butte have now
provided a handy roadmap for those contem-
plating a foray into the world of microarrays.
Microarrays for an Integrative Genomics
represents the collective wisdom of experi-
enced investigators in this emerging field.
The book is divided into seven self-contained
sections that discuss the advantages and
disadvantages of microarray experiments, ex-
perimental design, and data analysis in an
integrated manner. The text is an easy read:
I was able to finish the book in a weekend
of concentrated reading. Figures are illustra-
tive and well labeled. As with all books that
attempt to discuss a fast-moving field, the
reference list contains important articles in
the field but is not comprehensive. Similarly,
while most important themes are touched on,
there is a bit of unevenness to the discussion
that almost inevitably reflects the biases of
the authors. In particular, much of the science
and art of microarray experimentation in-
volves data analysis. While it is not practical
to discuss every algorithm or approach used
in this type of data mining, it would have been
useful to discuss results from published stud-
ies in the context of the algorithms presented
to give the reader a feel for what they should
look for as they scan the microarray litera-
ture. A more in-depth discussion of the statis-
tical issues surrounding this type of data
analysis is also lacking. Who should read this
book? Graduate students, research fellows,
and investigators from outside of the func-
tional genomics field will find lots of useful
information in this work; experienced in-
vestigators may find much of the discussion
elementary. Notwithstanding these minor
issues, the authors have produced a very
nice work that will prove useful to many
aspiring genomicists.
SRIDHAR RAMASWAMY
Whitehead Institute
MIT Center for Genome Research
Cambridge, Massachusetts and
Department of Medical Oncology
Dana-Farber Cancer Institute
Harvard Medical School
Boston, Massachusetts
DOI: 10.1002/ajhb.20009
The X in Sex: How the X Chromosome
Controls Our Lives. By David Bainbridge.
Cambridge, MA: Harvard University Press.
2003. $22.95 (Cloth).
Why are men and women different? What
are the evolutionary origins and consequences
ofthesedifferences?Whyareconditionssuch
as hemophilia, muscular dystrophy, and color
blindness largely limited to males? Why is color
blindness almost always red–green and almost
never blue–yellow? What happens when a
woman is born with a single X? Why is it that
mainly women suffer from autoimmune dis-
eases? Why aren’t female identical twins truly
identical? For that matter, why aren’t all of a
female’s cells truly identical? The critical fac-
tor, argues David Bainbridge, is the X chromo-
some. In particular, the fact that women have
two, while men have but one X and a solitary,
diminutive Y.
In ‘The X in Sex,’ author Dr. Bainbridge, a
clinical anatomist and Fellow at St. Catharine’s
College, University of Cambridge, explores how
BOOK REVIEWS 175
our sex chromosomes determine our gender as
well as many of our other physical features and
afflictions. Written for the general public, this
easy-to-read book is an informative and enter-
taining exploration of the biology, cultural his-
tory, and scientific discovery of the X chromo-
some.
The book is divided into three major chap-
ters that broadly cover the discovery and evo-
lution of the sex chromosomes (X and Y), the
X-linked diseases that predominantly affect
men, and X-related issues that are unique
to women. In the first chapter, ‘Making a
Difference,’ we learn that the sex chro-
mosomes evolved from a pair of ordinary
autosomes, as well as how and why the Y-
chromosome teeters on the edge of extinction.
We soon discover that it is the Y chromosome,
the male chromosome, and specifically the
‘Sry’ gene on that chromosome, that actively
begins the cascade of events that turns undif-
ferentiated cells into a male. However, that
fact, like the Y-chromosome, is but a smallish
piece of the story. After all, men and women
have countless other physical differences in
addition to the more obvious distinctions
associated with procreation.
Subsequent chapters describe how the
genes on the X chromosome act differently
from genes on the autosomes. These differ-
ences have the effect—among other conse-
quences—of differentially causing disease in
men (because a single deleterious gene on the
X has no sister to mask its effects) as wellas in
women (one of the risks of inactivating one of
the female’s X chromosomes). In ‘The Duke
of Kent’s Testicles,’ we are introduced to X-
linked diseases with the example of hemophi-
lia that includes the genealogy of the Houses
of Hanover while describing the potential
deadly consequences of a single X. From
there we learn about other X-linked diseases
(specifically, manifestation of color blindness
and muscular dystrophy) with varying levels
or morbidity and lethality. Through cross-
comparison, each of these examples further
illustrates the various consequences and vary-
ing patterns of expression of the single X. The
final major chapter, ‘The Double Life of
Women,’ explores the potential ill effects of
and evolved mechanism for dealing with two
X chromosomes in women. In this final major
chapter, Bainbridge recalls and then deftly
weaves together concepts, observations, and
lessons from previous sections.
These major chapters are interposed with
helpful interludes that reinforce key ele-
ments of the current and coming discourse.
Replete with a glossary and suggested read-
ings keyed to major subheadings, this well-
indexed volume takes us from discovery to
speculation and back. Along the way, David
Bainbridge cleverly introduces key terms in
appropriate contexts using very accessible
definitions.
Although peppered with humor, Bain-
bridge never loses sight of the seriousness of
this subject. Nowhere is this more certain
than in the final section, an epilog that
focuses on sex ratios, gender preferences,
and the technological and societal issues
therein. Indeed, throughout the book Bain-
bridge skillfully relates biology to the history
of the science, telling the entire story within
the context of the interplay between science
and society. While some of the playfully dis-
paraging discussion of the Y chromosome may
require modification based on recent re-
search, these revelations do not diminish the
essential points of this work—a volume that
I highly recommend.
KEVIN M. KELLY
Departments of Anthropology and
Community & Behavioral Health
University of Iowa
Iowa City, Iowa
DOI: 10.1002/ajhb.20010
Sexual Selection and Reproductive Compe-
tition in Primates: New Perspectives and
Directions. Edited by Clara B. Jones. xx +
647 pp. Norman, OK: American Society of
Primatologists. 2003. $60.00 ($45.00 for
ASP members) (Paper).
It has been more than 130 years since the
publication of Darwin’s (1871) The Descent
of Man, and Selection in Relation to Sex.In
that work, he elaborates on the concept of
sexual selection—briefly introduced in On
the Origin of Species (Darwin, 1859)—and
specifically outlines and provides examples
of adaptations that evolved through the
struggle with conspecifics for reproductive
opportunity and resources (e.g., mates), a
struggle that determines who reproduces
and who does not and often results in the
evolution of sex differences. Darwin empha-
sized the influence of male–male compe-
tition (intrasexual competition) over access
to mates and female choice (intersexual
176 BOOK REVIEWS
choice) of mating partners, although he also
discussed the importance of male choice in
humans. As described by Cronin (1991) and
the chapter by Shahnoor and Jones (first
chapter), Darwin’s theory of sexual selection
languished in the biological sciences for
about 100 years. In the 1970s, conceptual
advances highlighted the importance of par-
enting (Trivers, 1972) and ecological (Emlen
and Oring, 1977) conditions on reproductive
strategy, and with this helped to renew
interest in sexual selection. On the basis of
these conceptual elaborations and subse-
quent field and laboratory studies, we now
understand the influence of intrasexual
competition and intersexual choice on the
evolution and expression of sexual differ-
ences in many species (Andersson, 1994).
Unfortunately, and as noted in Nunn’s
concluding chapter, primatologists have not
taken full advantage of Darwin’s organizing
framework and, as a result, less is known
about sexual selection in primates than in
many other species. Within this historical
context, Jones’ edited volume and each of
the chapters therein can be fully appreciated
as important and much-needed theoretical
and empirical tests and elaborations on
Darwin’s original ideas. Excluding Nunn’s
insightful overview and prospectus, the re-
maining 18 chapters are organized into four
sections. In addition to Shahnoor’s and Jones’
chapter on the history of sexual selection in
primatology, each chapter in the first section
addresses important theoretical issues and
provides directions for future research on
the proximate expression of sexual selection
in primates. Included among these is Strier’s
discussion of the importance of population
demography (e.g., sex ratio); Hager’s focus
on reproductive skew (i.e., degree of within-
sex differences in reproductive success);
Jones’ and Agoramoorthy’s review of alterna-
tive reproductive strategies; and Gerald’s dis-
cussion of sex differences in coloration (e.g.,
genitalia) as potentially related to intrasexual
competition and intersexual choice.
The second section provides a much-wel-
comed quartet of chapters on reproductive
strategies and competition among females,
an issue that was not well addressed in The
Descent of Man (Darwin, 1871). Watson and
colleagues take a life history perspective on
the female reproductive strategy of Garnett’s
bushbabies (Otelemur garnettii), that is, the
tendency for young, primiparous mothers to
produce many more male (70%) than female
offspring. The pattern is considered in terms
of ultimate (e.g., resource competition with
female offspring), and proximate (e.g., hormo-
nal) mechanisms. Saltzman provides a thor-
ough discussion of reproductive competition
among female marmosets (Callithrix jacchus)
through inhibition of ovarian function in sub-
ordinate females and infanticide by dominant
females. Female coalitions in bonobos (Pan
paniscus) are often discussed, but the darker
side of relationships among these females are
not. Vervaecke’s and colleague’s chapter pro-
vides a nice counter to this trend, with dis-
cussion of how dominant bonobo females
interfere with the copulations (with males)
of subordinate females and may harass the
offspring of these subordinates. The section
ends with Reeder’s important and thorough
discussion of the many ways in which cryptic
female choice (e.g., sperm competition) may
operate in primates.
The third section includes chapters that go
beyond the standard physical contests among
males for access to estrous females, includ-
ing Heymann’s discussion of the relations
among male choice, female–female competi-
tion, and paternal care in Callitrichines;
Crockett’s assessment of the infanticidal
behavior of red howler (Alouatta) males,
and Palombit’s similar analysis for various
species of savanna baboon (Papio); Setchell’s
analysis of different reproductive morphs in
mandrills (Mandrillus sphinx) and orangu-
tans (Pongo pygmaeus); and Thomsen and
colleague’s assessment of the potential func-
tion of male masturbation (i.e., sperm com-
petition). Each of these chapters is note-
worthy in the use of field and other data to
test alternative hypotheses regarding the
ultimate (e.g., to induce estrous) or not
(e.g., social pathology) function of these fea-
tures of male reproductive behavior. The
final section includes chapters that examine
ecological (Bicca-Marques) and socioecologi-
cal (Robbins; Bergman and Beehner) condi-
tions that may influence the operation of
sexual selection or may yield alternative
explanations, such as species recognition
(Froehlich), for phenomena normally consid-
ered under the preview of sexual selection.
Each of these chapters makes an important
contribution to our understanding of theo-
peration of sexual selection in a wider con-
text.
In all, Darwin would have been pleased by
the contributions to this volume, and by the
progress that has, at long last, been made in
BOOK REVIEWS 177
the area of sexual selection and its applica-
tion to primates. The only disappointment
was the lack of a separate chapter or chap-
ters on sexual selection in modern humans
and during hominid evolution (e.g., as
indexed by sexual dimorphisms).
LITERATURE CITED
Andersson M. 1994. Sexual selection. Princeton, NJ:
Princeton University Press.
Cronin H. 1991. The ant and the peacock. New York:
Cambridge University Press.
Darwin C. 1859. On the origin of species by means of
natural selection. London: John Murray.
Darwin C. 1871. The descent of man, and selection in
relation to sex. London: John Murray.
Emlen ST, Oring LW. 1977. Ecology, sexual selection, and
the evolution of mating systems. Science 197:215–223.
Trivers RL. 1972. Parental investment and sexual selec-
tion. In: Campbell B, editor. Sexual selection and
the descent of man 1871–1971. Chicago: Aldine.
p 136–179.
DAVID C. GEARY
Department of Psychological Sciences
University of Missouri Columbia
Columbia, Missouri
DOI: 10.1002/ajhb.20011
178 BOOK REVIEWS
... However, during the last decade, it has become increasingly known that primate males of a considerable variety of species masturbate as a common component of their sexual behaviour. Particularly in macaques, mangabeys , baboons and guenons, male masturbation is, beside heterosexual copulations, probably the most frequently observed sexual behaviour (Thomsen et al. 2003; Frearson 2005; Dixson 2012 ). This offers the possibility of estimating semen volumes by direct observation (Thomsen and Soltis 2004; Inoue 2012 ) and to determine male fertility under field conditions. ...
... Macaque males masturbate with their hands (Fig. 1a and b; Thomsen et al. 2003; Thomsen and Soltis 2004; Inoue 2012). Whenever males were seen to masturbate sitting on the ground (earth, rocks, tarmac, etc.) volumes of the ejaculated semen were estimated (Fig. 1c). ...
... Masturbation by males has been reported in approximately 60 primate species to date. It occurs in 91 % of cercopithecoid genera (Thomsen et al. 2003; Dixson 2012). Beside macaques, baboons (Papio spp.), mandrills (Mandrillus sphinx) and drills (M. ...
Article
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Assessments of primate male fertility via semen analyses are so far restricted to captivity. This study describes a non-invasive method to collect and analyse semen in wild primates, based on fieldwork with Yakushima macaques (Macaca fuscata yakui). Over nine mating seasons between 1993 and 2010, 128 masturbatory ejaculations were recorded in 21 males of 5 study troops, and in 11 non-troop males. In 55 %, ejaculate volume was directly estimated, and in 37 %, pH-value, sperm vitality, numbers, morphology and swimming velocity could also be determined. This approach of assessing semen production rates and individual male fertility can be applied to other primate taxa, in particular to largely terrestrial populations where males masturbate frequently, such as macaques and baboons. Furthermore, since explanations of male reproductive skew in non-human primate populations have until now ignored the potential role of semen quality, the method presented here will also help to answer this question.
... Masturbation, or self-manipulation of the genitalia, is part of the natural behavioral repertoire of many animal species (reviewed in Bagemihl 1999; Thomsen et al. 2003;Dixson 2012), including humans (Laqueur 2003;Dixson 2012), but whether this behavior has an adaptive function is still poorly understood. Although comparative behavioral data on masturbation could help us understand the adaptive function and evolution of this behavior, very few data are available to date. ...
... This by-product hypothesis implies that males do not gain any fitness benefits, in terms of their health or survival, or increased mating or reproductive success, from masturbation. Second, the 'ejaculate-qualityimprovement' hypothesis posits that masturbation is an adaptive behavior that serves to eliminate degraded gametes or avoid polyzoospermy in order to increase the overall ejaculate quality, thus increasing the probability of impregnation when males copulate with a fertile female ( Zimmerman et al. 1965;Baker & Bellis 1993, 1995Thomsen et al. 2003;Thomsen & Soltis 2004). While suggesting very different functions of masturbation, these two hypotheses both predict that masturbation should be more frequent among males that have little or no opportunity to mate, and/or occur in periods of infrequent mating (Thomsen et al. 2003;Dixson & Anderson 2004;Thomsen & Soltis 2004;Waterman 2010;Dixson 2012). ...
... Second, the 'ejaculate-qualityimprovement' hypothesis posits that masturbation is an adaptive behavior that serves to eliminate degraded gametes or avoid polyzoospermy in order to increase the overall ejaculate quality, thus increasing the probability of impregnation when males copulate with a fertile female ( Zimmerman et al. 1965;Baker & Bellis 1993, 1995Thomsen et al. 2003;Thomsen & Soltis 2004). While suggesting very different functions of masturbation, these two hypotheses both predict that masturbation should be more frequent among males that have little or no opportunity to mate, and/or occur in periods of infrequent mating (Thomsen et al. 2003;Dixson & Anderson 2004;Thomsen & Soltis 2004;Waterman 2010;Dixson 2012). In addition, the ejaculate-quality-improvement hypothesis predicts that males who have infrequent access to females but masturbate frequently should have higher sperm quality and higher probability of impregnation when compared to males who masturbate less frequently, other things being equal. ...
Article
The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non-human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale-multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non-functional by-product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free-ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower-ranking males mated less and tended to masturbate more frequently than higher-ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.
... Though male and female members of each species or subspecies within this genus are difficult to distinguish based on size and morphological features, many species of gibbon are sexually dichromatic. Pelage changes occur mostly at sexual maturation, making it easier to identify one sex from another as well as identifying sexually mature form from sub adult (Geary 2004). ...
Thesis
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Hominoid primate species differ remarkably in their social grouping and mating systems, notably including differing degrees of post-copulatory sexual selection. As the mating system of extinct hominins remains unknown and difficult to predict, it may be useful to examine more proximate phenotypes correlated with behavior. For example, chimpanzees and bonobos have a large ejaculate that coagulates into a rigid copulatory plug, presumably in response to high levels of sperm competition, while gorillas have a small semi-viscous ejaculate associated with low sperm competition. To understand the molecular basis responsible for differences in semen biochemistry among hominoid species, I completed two research projects. First, by cloning the upstream putative promoters of the chimpanzee, bonobo, human, and gorilla prostatic acid phosphatase ( ACPP) genes into luciferase reporter vectors followed by transient transfections into a human prostate cell line, I identified the underlying nucleotide changes that reduce expression of this protein in chimpanzee semen. Second, by mapping large deletions at the kallikrein-related peptidase (KLK) locus in the gorilla and gibbon genomes, I characterized the convergent gene loss and the formation of a novel chimeric gene in these monandrous species. For both the ACPP and KLK locus changes, I determined the polarity of the changes through outgroup comparison. At ACPP, the reduced expression in chimpanzee and bonobo is derived, and likely in response to the onset of intense sperm competition in the common ancestor of these two species. If this biochemical phenotype is indeed a proxy for mating behavior, my data provides some evidence (to be compared and contrasted with other molecular, behavioral, and paleontological data) that the last common ancestor of humans and chimpanzees was not chimp-like in its high degree of polyandry.
... Casos de infanticídios em primatas têm sido relatados tanto para os da subordem Strepsirhini quanto para os da subordem Haplorhini. Em relação a infraordem Platyrrhini (primatas do novo mundo), muito se discute sobre a existência e a natureza desse comportamento no gênero Alouatta Lacépede, 1799, ocorrendo relatos para A. pigra Lawrence, 1933(KNOPFF et al. 2004, A. seniculus (Linnaeus, 1766) (RUDRAN 1979, AGARAMOORTHY & RUDRAN 1995, PALACIOS 2000, A. palliata (Gray, 1849) (CLARKE 1983), A. guariba (Humboldt, 1812) (GALETTI et al. 1994) e A. caraya (Humboldt, 1812) (ZUNINO et al. 1985), porém os casos relatados são raros (CROCKETT 2003). Três principais hipóteses para a existência deste comportamento são propostas: as hipóteses adaptativas, como a de seleção sexual (SUGIYAMA 1967, HRDY 1974) e a de competição por recurso (AGORAMOORTHY & RUDRAN 1995) e a não adaptativa, a de patologia social (SUSSMAN et al. 1995). ...
Article
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This work reports on an infanticide attempt by a dominant resident male in a group of Alouatta caraya (Humboldt, 1812) on an extra-group infant in an Island in the Paraná river, Paraná, Brazil. The encounter of an infant-female pair with a resident male was brought about by human interference. Give the circumstances in which the event ocurred and the hierarchical position of the agressor, the social pathology hypothesis seems the most plausible explanation for such behavior.
Chapter
Male and female primates from all extant radiations engage in autosexual behaviors, implying that masturbation is a facet of the sexual repertoire of our hominid ancestors. At a proximate level, masturbation results in relaxation and reduced aggressiveness. At an ultimate level, male masturbation might be beneficial because old and low-quality sperm are discarded, while fresh sperm production is stimulated. Convincing functional explanations for female masturbation are still lacking.
Article
In the present study, we aimed to assess the influence of different social contexts on the seminal coagulation and sperm quality in captive tufted capuchin monkeys. For this, males were housed either individually, in mixed-sex groups (with females), or in male-only groups. Monkeys were housed in cages and each cage type (i.e., individual or group cage) was placed in a different room. Forty-one males were subjected to semen collection by rectal electroejaculation. The degree of seminal coagulation was determined on a scale of I–IV. Seminal volume, sperm concentration, sperm motility, vigor, and plasma membrane integrity were evaluated for all ejaculate samples. All ejaculates collected showed degrees of coagulation between II and IV, where the majority presented coagulation degree IV, when collected from animals housed in groups. No statistical differences among percentages of coagula degree when samples were collected from males housed individually. Animals housed in group cages (male-only groups and mixed-sex groups) showed a significantly higher percentage of ejaculates at degree IV than males housed individually. Seminal volume was not affected by the coagula degree but by the housing system, where animals housed individually showed the highest volume (543 μl) when compared with those animals from male (273 μl) and mixed-sex (318 μl) groups. No differences were observed in semen volume when comparing male-only groups with mixed-sex groups. Sperm motility was affected by both housing system and coagula degree. Samples with coagula degree IV from animals housed individually showed the highest (72%) sperm motility percentages. Sperm plasma membrane integrity was lower when samples were presenting coagula degree II + III and collected from male- (17%) or mixed-sex (23%) groups. However, this housing system effect was not observed when sperm was obtained from coagula degree IV semen. Sperm vigor was neither affect by housing system or coagula degree.
Article
Sexual selection has become a major focus in evolutionary and behavioral ecology. It is also a popular research topic in primatology. I use studies of mandrills (Mandrillus sphinx), a classic example of extravagant armaments and ornaments in animals, to exemplify how a long-term, multidisciplinary approach that integrates field observations with laboratory methods can contribute to on-going theoretical debates in the field of sexual selection. I begin with a brief summary of the main concepts of sexual selection theory and the differences between the sexes. I then introduce mandrills and the study population and review mandrill life history, the ontogeny of sex differences, and maternal effects. Next, I focus on male-male competition and female choice, followed by the less well-studied questions of female-female competition and male choice. This review shows how different reproductive priorities lead to very different life histories and divergent adaptations in males and females. It demonstrates how broadening traditional perspectives on sexual selection beyond the ostentatious results of intense sexual selection on males leads to an understanding of more subtle and cryptic forms of competition and choice in both sexes and opens many productive avenues in the study of primate reproductive strategies. These include the potential for studies of postcopulatory selection, female intrasexual competition, and male choice. These studies of mandrills provide comparison and, I hope, inspiration for studies of both other polygynandrous species and species with mating systems less traditionally associated with sexual selection. Am J Phys Anthropol 159:S105-S129, 2016. © 2016 Wiley Periodicals, Inc.
Article
Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: X² = 27.43, df = 3, p < 0.0001; 2001: X² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4-9 yrs), or 2) were older females (=10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.
Article
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Male mammals often kill conspecific offspring. The benefits of such infanticide to males, and its costs to females, probably vary across mammalian social and mating systems. We used comparative analyses to show that infanticide primarily evolves in social mammals in which reproduction is monopolized by a minority of males. It has not promoted social counterstrategies such as female gregariousness, pair living, or changes in group size and sex ratio, but is successfully prevented by female sexual promiscuity, a paternity dilution strategy. These findings indicate that infanticide is a consequence, rather than a cause, of contrasts in mammalian social systems affecting the intensity of sexual conflict.
Data
Auto-sexual behaviour (masturbation) is the most common sexual activity of humans, but surprisingly little is known about how it evolved and why it occurs. For centuries, masturbation has been considered taboo or regarded as an unnatural and even pathologic behaviour (Laqueur 2004). During the last decade however, it has been revealed that masturbation is a common part of the sexual repertoire in non-human primate populations as well. Masturbation is more prevalent in species that exhibit a polygynandrous (multi-male, multi-female) breeding system but it also occurs in harems and in solitary taxa. This suggests that masturbation is an ancestral, phyologenetically widespread trait within the order of primates and further implies that it is a facet of our own hominid ancestor's sexual repertoire (Thomsen et al. 2003). In around 80 species from all major radiations of the living anthropoid primates, males were observed to exhibit masturbatory behaviours that slightly differ in some peculiarities. In several species of New World monkeys, Old World monkeys, lesser apes and great apes, males are reported to masturbate frequently using their hands, feet or mouth to stimulate their genitals until ejaculation occurs. In prosimians, one of the most evolutionarily ancient primate taxon, masturbation is known in mouse lemurs and galagos. In females, masturbation is described in 50 primate species (Jones 2005). Females exhibit more sophisticated kinds of masturbatory behaviours than males. Besides the whole ano-genital region they include stimulation of the breast region using various substrates. Females of species that are known for the use of tools use "tool-like" objects to masturbate. Orang-utans prepare sticks of adequate size, bonobos use pieces of lianas and capuchin monkeys use plant parts for vaginal stimulation. However, it is more difficult to rate the level of arousal in females. Vocalisation, distinctive facial expressions or excitement visibly occur in some taxa (macaques, cebids, guenons), but usually female orgasm (if any) seems concealed.
Article
In the current resurgence of interest in the biological basis of animal behavior and social organization, the ideas and questions pursued by Charles Darwin remain fresh and insightful. This is especially true of The Descent of Man and Selection in Relation to Sex, Darwin's second most important work. This edition is a facsimile reprint of the first printing of the first edition (1871), not previously available in paperback. The work is divided into two parts. Part One marshals behavioral and morphological evidence to argue that humans evolved from other animals. Darwin shoes that human mental and emotional capacities, far from making human beings unique, are evidence of an animal origin and evolutionary development. Part Two is an extended discussion of the differences between the sexes of many species and how they arose as a result of selection. Here Darwin lays the foundation for much contemporary research by arguing that many characteristics of animals have evolved not in response to the selective pressures exerted by their physical and biological environment, but rather to confer an advantage in sexual competition. These two themes are drawn together in two final chapters on the role of sexual selection in humans. In their Introduction, Professors Bonner and May discuss the place of The Descent in its own time and relation to current work in biology and other disciplines.
Book
Why have males in many species evolved more conspicuous ornaments and signals such as bright colours, enlarged fins, and feather plumes, as well as larger horns and other weapons than females? Darwin's explanation for such secondary sex traits, the theory of sexual selection, became his scientifically perhaps most controversial idea. It suggests that the traits are favoured by competition over mates. After a long period of relative quiescence, theoretical and empirical research on sexual selection has erupted during the last decades. This book describes the theory and its recent development, reviews models, methods, and empirical tests, and identifies many remaining open problems. Among the topics discussed are the selection and evolution of mating preferences; relations between sexual selection, species recognition, and speciation; constraints on sexual selection; the selection of secondary sex differences in body size, weapons, and in visual, acoustic, and chemical signals. The rapidly growing study of sexual selection in plants is also reviewed. Other chapters deal with alternative mating tactics, and with the relationships among sexual selection, parental roles, and mating systems. The present review of this very active research field will be of interest to students, teachers, and research workers in behavioural and evolutionary ecology, animal behaviour, plant reproductive ecology, and other areas of evolutionary biology where sexual selection is a potential selection factor. In spite of much exciting progress, some of the main questions in the theory of sexual selection yet remain to be answered.
Sexual selection and the descent of man 1871-1971
  • R L Trivers
Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man 1871-1971. Chicago: Aldine. p 136-179.