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Environmental shifts and life-history changes may result in formerly adaptive traits becoming non-functional or maladaptive. In the absence of pleiotropy and other constraints, such traits may decay as a consequence of neutral mutation accumulation or selective processes, highlighting the importance of natural selection for adaptations. A suite of traits are expected to lose their adaptive function in asexual organisms derived from sexual ancestors, and the many independent transitions to asexuality allow for comparative studies of parallel trait maintenance versus decay. In addition, because certain traits, notably male-specific traits, are usually not exposed to selection under asexuality, their decay would have to occur as a consequence of drift. Selective processes could drive the decay of traits associated with costs, which may be the case for the majority of sexual traits expressed in females. We review the fate of male and female sexual traits in 93 animal lineages characterized by asexual reproduction, covering a broad taxon range including molluscs, arachnids, diplopods, crustaceans and eleven different hexapod orders. Many asexual lineages are still able occasionally to produce males. These asexually produced males are often largely or even fully functional, revealing that major developmental pathways can remain quiescent and functional over extended time periods. By contrast, for asexual females, there is a parallel and rapid decay of sexual traits, especially of traits related to mate attraction and location, as expected given the considerable costs often associated with the expression of these traits. The level of decay of female sexual traits, in addition to asexual females being unable to fertilize their eggs, would severely impede reversals to sexual reproduction, even in recently derived asexual lineages. More generally, the parallel maintenance versus decay of different trait types across diverse asexual lineages suggests that neutral traits display little or no decay even after extended periods under relaxed selection, while extensive decay for selected traits occurs extremely quickly. These patterns also highlight that adaptations can fix rapidly in natural populations of asexual organisms, in spite of their mode of reproduction.
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Biol. Rev. (2014), pp. 000000. 1
doi: 10.1111/brv.12078
On the fate of sexual traits under asexuality
Casper J. van der Kooi and Tanja Schwander,†
Center for Ecological and Evolutionary Studies, University of Groningen, 9700CC, Groningen, The Netherlands
ABSTRACT
Environmental shifts and life-history changes may result in formerly adaptive traits becoming non-functional or
maladaptive. In the absence of pleiotropy and other constraints, such traits may decay as a consequence of neutral
mutation accumulation or selective processes, highlighting the importance of natural selection for adaptations. A suite
of traits are expected to lose their adaptive function in asexual organisms derived from sexual ancestors, and the
many independent transitions to asexuality allow for comparative studies of parallel trait maintenance versus decay. In
addition, because certain traits, notably male-specific traits, are usually not exposed to selection under asexuality, their
decay would have to occur as a consequence of drift. Selective processes could drive the decay of traits associated with
costs, which may be the case for the majority of sexual traits expressed in females. We review the fate of male and female
sexual traits in 93 animal lineages characterized by asexual reproduction, covering a broad taxon range including
molluscs, arachnids, diplopods, crustaceans and eleven different hexapod orders. Many asexual lineages are still able
occasionally to produce males. These asexually produced males are often largely or even fully functional, revealing
that major developmental pathways can remain quiescent and functional over extended time periods. By contrast,
for asexual females, there is a parallel and rapid decay of sexual traits, especially of traits related to mate attraction
and location, as expected given the considerable costs often associated with the expression of these traits. The level of
decay of female sexual traits, in addition to asexual females being unable to fertilize their eggs, would severely impede
reversals to sexual reproduction, even in recently derived asexual lineages. More generally, the parallel maintenance
versus decay of different trait types across diverse asexual lineages suggests that neutral traits display little or no decay
even after extended periods under relaxed selection, while extensive decay for selected traits occurs extremely quickly.
These patterns also highlight that adaptations can fix rapidly in natural populations of asexual organisms, in spite of
their mode of reproduction.
Key words: trait decay, regressive evolution, sexual traits, asexuality, parthenogenesis.
CONTENTS
I. Introduction ................................................................................................ 1
II. Processes underlying trait decay ............................................................................ 2
III. Decay of sexual traits in asexual lineages ................................................................... 2
IV. Testing for decay of sexual traits ........................................................................... 3
V. Fate of male-specific traits in asexual lineages .............................................................. 8
VI. Fate of female sexual traits in asexuals ...................................................................... 9
VII. Genetic architecture of decayed traits ...................................................................... 11
VIII. Conclusions ................................................................................................ 11
IX. Acknowledgements ......................................................................................... 12
X. References .................................................................................................. 12
I. INTRODUCTION
Studies on how natural selection favours adaptations typically
focus on the evolution of novel traits (e.g. Cracraft, 1990;
Moczek, 2008; Brakefield, 2011; Moczek et al., 2011).
* Author for correspondence (Tel: +41 21 692 4151; E-mail: tanja.schwander@unil.ch).
Present address: Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
However, the fate of traits that no longer contribute
to fitness can also highlight the importance of natural
selection for the maintenance of adaptations (Fong, Kane
& Culver, 1995; Wiens, 2001; Porter & Crandall, 2003;
Lahti et al., 2009). Formerly adaptive traits may become
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
2Casper J. van der Kooi and Tanja Schwander
non-functional, or even maladaptive, as a consequence of
environmental shifts or changes in life history, accompanied
by changes in selective pressures (Fong et al., 1995; Lahti
et al., 2009). Such traits often decay, i.e. become reduced
or disappear completely, a process sometimes referred to as
vestigialization.
Vestigialization is a form of regressive evolution, which
may be an order of magnitude more frequent than the
evolution of novel traits (Fong et al., 1995). Prominent
examples for vestigialization are found in the parallel eye and
pigment loss in a range of cave-dwelling organisms (Wilkens
& Strecker, 2003; Jeffery, 2009; Protas, Trontelj & Patel,
2011), reduced wings of flightless birds (McNab, 1994), or loss
of innate defence behaviours in the absence of the relevant
threats (e.g. Coss, 1999; Lahti, 2006). Less conspicuous
than vestigialization of morphological or behavioural traits,
regressive evolution has also been uncovered for physiological
and metabolic pathways. For example, fat synthesis has
decayed in parallel in different parasitoid wasps, most likely
because the constant availability of host-produced lipids
rendered the parasitoids’ own synthesis pathways redundant
(Visser et al., 2010). Other ‘cryptic’ examples of regressive
evolution stem from hosts becoming dependent on formerly
parasitic bacteria for such fundamental processes as oocyte
development or sex differentiation (Dedeine et al., 2001;
Zchori-Fein, Borad & Harari, 2006; Timmermans & Ellers,
2008; Kageyama, Narita & Watanabe, 2012).
Trait decay is not necessarily accompanied by
degeneration of the molecular pathways underlying the
development of its functional version. Maintenance of
pathways may stem, for example, from pleiotropy where the
same gene networks function in several processes (Fong et al.,
1995). Thus, even if a character is phenotypically absent,
the genetic information responsible for its development
can remain quiescent, occasionally resulting in character
expression.
II. PROCESSES UNDERLYING TRAIT DECAY
Atraitcandecayvia different processes, depending on
whether the formerly adaptive trait is neutral or maladaptive
in the new selective environment (Fong et al., 1995; Hall
& Colegrave, 2008). In the first case, the trait would be
under relaxed selection whereby trait-affecting mutations
that would have been removed by selection under the past
conditions may accumulate and fix via drift (e.g. Lande, 1978;
Hall & Colegrave, 2008; Lahti et al., 2009). This process of
decay, often referred to as neutral mutation accumulation,
would be expected to proceed slowly (Teot´
onio & Rose,
2000; Hall & Colegrave, 2008).
In the second case, if a formerly adaptive trait becomes
maladaptive in a new selective environment, the trait would
be expected to regress rapidly, driven by selection for reduced
trait expression (Hall & Colegrave, 2008). Decay would then
proceed until the character is gone, or simplified to an
intermediate stage where further reduction is no longer
adaptive (Prout, 1964; Fong et al., 1995; Zuk, Rotenberry
& Tinghitella, 2006). Such trait reduction could also be
selected for indirectly if the reduction of a useless trait
releases constraints on functions that contribute to fitness
and/or allows for reallocation of limited resources (Prout,
1964; Regal, 1977; Fong et al., 1995; Eckert, 2001; Dorken,
Neville & Eckert, 2004).
A major challenge for studies of trait decay in natural
populations has been to disentangle neutral from selective
processes driving the reduction of specific traits. A successful
approach to demonstrating selective processes has been the
analysis of traits with variable expression whereby selection-
driven decay is revealed by fitness benefits in individuals with
strongly reduced expression (Eckert, 2001; Dorken et al.,
2004). In many cases however, there is little variation among
individuals in the level of trait reduction, and a similar
approach could not provide positive evidence for decay
driven by neutral mutation accumulation.
Part of the difficulty in identifying processes underlying
trait decay stems from a lack of information on the costs
of traits and genetic correlations among them, as well as a
lack of parallel trait losses (Lahti et al., 2009). Here, we show
that regressive evolution of sexual traits in parthenogenetic
all-female lineages (hereafter referred to as asexual lineages)
can provide insights into both decay via drift and selective
processes. Indeed, the many independent origins of asexual
lineages from sexual ancestors in a broad range of taxa
allow for comparative studies of trait decay. In addition,
an exceptionally large range of sexual traits, including
physiological, behavioural and morphological traits should
be affected by transitions to asexuality. As a consequence,
the fate of (putatively) neutral as well as highly costly traits
can be investigated.
III. DECAY OF SEXUAL TRAITS IN ASEXUAL
LINEAGES
In the transition from sexual reproduction with separate
male and female sexes to asexuality in all-female lineages,
many formerly adaptive traits should lose their adaptive
value (Carson, Chang & Lyttle, 1982). These sexual traits
range from traits involved in mate location and attraction, to
courtship and copulation behaviours, to traits specific to the
male sex (e.g. Carson et al., 1982; Pannebakker et al., 2004;
Lehmann et al., 2011; Fig. 1).
Because certain sexual traits are not expressed at all in
asexuals, these traits should only decay as a consequence of
drift. Prime candidates for such neutral traits would be any
trait specific to males. Most asexual lineages either produce
no males at all, or if they do, the extremely rare ‘accidental
males’ appear to have no mating opportunities or success
in natural populations (e.g. Gottlieb & Zchori-Fein, 2001;
Sch¨
on, Rossetti & Martens, 2009; Mirab-Balou & Chen,
2010; Schwander et al., 2013). Thus, male-specific traits are
either not expressed, or are only expressed in individuals
that have zero fitness (the males). In both cases, male-specific
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
On the fate of sexual traits under asexuality 3
Fig. 1. Sexual traits expected to be under relaxed or negative
selection in asexuals. Drawings courtesy of Laurent Bes.
traits are not exposed to selection and could therefore only
regress at a neutral rate.
In contrast to the male-specific traits, female-expressed
traits formerly involved in mate attraction are unlikely to be
neutral in asexuals. In addition to energy costs associated
with the production of mate-attraction signals, pheromones
and acoustic signals are prime targets for predators and
parasitoids to locate their prey (e.g. Zuk & Kolluru, 1998;
Zuk et al., 2006). Thus, the production of such signals should
be under strong negative selection in asexual females, where
mate attraction is superfluous.
Here, we review the fate of sexual traits in animal species
characterized by asexual reproduction. A literature survey
for descriptions of male and/or female sexual traits in
asexual lineages allowed us to obtain information for 93
asexual lineages, representing a diversity of taxa from 11
different hexapod orders, diplopods, arachnids, crustaceans
and molluscs (Table 1). By investigating different trait
categories across independently derived asexual lineages,
we develop insights into trait decay via drift and selection.
We focus on asexual all-female species deriving from sexual
ancestors with separate sexes, to standardize comparisons
between the male and female sex. We further exclude cases
of asexuality where successful reproduction is dependent on
individuals of the opposite sex, as is the case for different
types of sperm-dependent parthenogenesis (e.g. Lamatsch &
St¨
ock, 2009) or male asexuality (e.g. Foucaud et al., 2007;
Hedtke et al., 2008). In these cases, individuals of the asexual
lineage still need to attract individuals of the opposite sex and
mate, such that costs and benefits associated with sexual traits
in these species should be more similar to sexual species than
to typical sperm-independent asexuals. We use unexpressed
traits, which are associated with little or no costs, to predict
the level of trait decay expected in the absence of selective
processes. By identifying parallel and rapid trait reductions
across organisms from very different ecological contexts,
we then highlight sexual traits that are universally costly in
natural populations of asexual lineages.
IV. TESTING FOR DECAY OF SEXUAL TRAITS
It is not possible to evaluate the functionality of a trait
that is not expressed (as is the case for male traits in
asexual lineages where no males are known and where
male production cannot be induced). For expressed sexual
traits, two approaches are used to investigate their decay in
an asexual lineage. First, it is sometimes possible to examine
a specific character directly via functional assays (for example
testing for sperm motility; Gottlieb & Zchori-Fein, 2001;
Zchori-Fein et al., 2001) or detailed histological examinations
(for example in spermathecae, evaluating the presence of
specific glandular tissues required for functional storage of
sperm; Gotoh et al., 2012). Alternatively, trait values for
asexuals are compared to corresponding values in the closest
sexual relatives whereby it is relevant to use appropriate
sexual references. Appropriate references are particularly
important when traits involving interactions between males
and females are assessed, which concerns many, if not most,
sexual traits. For example, to assess the production of mate-
attraction signals by asexual females, sexual males are used
as signal responders (Gottlieb & Zchori-Fein, 2001; Adachi-
Hagimori, Miura & Abe, 2011; Schwander et al., 2013). This
may pose a problem in some cases, given that sexual traits
can diverge rapidly between populations, such that reduced
sexual attractiveness of females to sexual males may be due
to population divergences rather than to reduced signal
production (i.e. decay) as a consequence of asexuality. In
such cases, comparisons among different sexual populations
can be useful to disentangle the effect of asexuality from
between-species divergences (Schwander et al., 2013).
Complementary information on sexual traits involving
interactions between females and males can be obtained
from males produced by females of some asexual species
(see Section V). In this case, detailed behavioural and
morphological observations are often necessary to distinguish
whether an apparent lack of a sexual function stems from
regressive evolution in females, males or both sexes such that
comparisons with sexual relatives may still be pertinent. In
addition, obtaining enough such asexually produced males
for replicated tests may be impossible, as often only a few
male individuals are known to occur in entire species (e.g.
Smith, Kamiya & Horne, 2006; Baur, 2010; Mirab-Balou &
Chen, 2010).
A notable exception to such sample limitation stems from
hymenopteran species in which asexuality is induced by
infection with bacterial endosymbionts (e.g. Stouthamer,
Luck & Hamilton, 1990a; Pannebakker et al., 2005; Kremer
et al., 2009). In sexual hymenopterans, unfertilized (haploid)
eggs develop into males whereas diploid eggs develop
into females (haplo-diploid sex determination). Thus virgin
sexual females produce exclusively haploid eggs giving rise
to sons. Females infected with parthenogenesis-inducing
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
4Casper J. van der Kooi and Tanja Schwander
Table 1. Case studies reporting on the functionality of sexual traits in asexual lineages deriving from sexual ancestors with separate sexes
Species information Summary Male traits Female traits
Taxonomic
groups and
species
names
Common
name
Parthenogenesis
Sex
determination in
sexual sister
groups
Male
Female
Male
produc-
tion
‘Normal’
morphology
Courting
behaviour/
attractive-
ness to
females
Mating
behaviour
Sperm
transfer/
sper-
matophore
production
Functional
sperm
Normal
spermath-
eca; seminal
receptacles
Mate
attraction;
response to
attraction;
courtship
Normal
copulation
behaviour;
sperm/
spermatophore
uptake
Egg
fertilization
References
ARTHROPODA
BRANCHIOPODA
Anostraca
Artemia parthenogenetica Brine shrimp A ZW:ZZ ? D Y Y Y Y N? Y N MacDonald & Browne (1987)
and Browne (1992)
MALACOSTRACA
Isopoda
Trichoniscus pusillus (elisabethae) Woodlouse A UnknownaD D Y Y Y Y N Y N Vandel (1931, 1934)
OSTRACODA
Limnocythere inopinata obl XX:XO? F? ? Y Y Geiger et al. (1998)
Vestalenula cornelia obl XX:XO? D? ? Y Y N?b Smith et al. (2006) and Sch¨
on
et al. (2009)
ARACHNIDA
Araneae
Coelotes troglocaecus Spider obl XX:XO ? D N? — Nc Shimojana & Nishihira (2000)
Dysdera hungarica Spider A XX:XO ? F? N? Y Korenko et al. (2007, 2009)
Theotima minutissimus Spider obl XX:XO ? D N? — Nc Edwards et al. (2003)
Triaeris stenaspis Spider obl XX:XO/XX:XY ? F? N? Y Burger (2009) and Korenko
et al. (2009)
Ixodida
Haemaphysalis longicornis (3n strain) Tick A XX:XO D D Y Y N N N N Oliver (1971) and Oliver et al.
(1973)
Sarcoptiformes
Platynothrus peltifer Oribatid mite obl UnknownaDD Y Y
d0e0eYN
c—0
eN Taberly (1987, 1988)
Nothrus palustris Oribatid mite obl UnknownaFD Y Y 0
e0eY—— 0
eN Taberly (1987, 1988)
Nothrus sylvestris Oribatid mite obl UnknownaF? D Y Y 0e0e——— 0
eN Taberly (1987, 1988)
Trhypochthonius tectorum Oribatid mite obl UnknownaDD Y Y
d0e0eYN
c—0
eN Taberly (1987, 1988)
Trombidiformes
Bryobia praetiosa Clover mite oblfHaplodiploid F D YfY — Y — — Y N Weeks & Breeuwer (2001)
Brevipalpus californicum Flat mite oblfHaplodiploid F? D YfY N Groot & Breeuwer (2006)
Brevipalpus obovatus Flat mite oblfHaplodiploid D D YfY Y N N Y N Groot & Breeuwer (2006)
Brevipalpus phoenicus False spider mite oblfHaplodiploid F? D YfY N Pijnacker et al. (1981) and
Groot & Breeuwer (2006)
DIPLOPODA
Nemasoma varicorne Millipede A XX:XO/XX:XY F D Y Y Y Y YgNc Enghoff (1967)
HEXAPODA
Collembola
Folsomia candida Springtail A XX:XO D D Y Y Y? N N N N? Kiauta (1970) and Buono
(2011)
Coleoptera
Cis fuscipes Beetle A XX:XY? ? D Y?hYh N N Lawrence (1967)
Diptera
Drosophila mercatorum Fruitfly A XX:XY ? D N? N Carson et al. (1982)
Ephemeroptera
Ameletus ludens Mayfly obl XX:XO? F? ? Y Y Funk et al. (2006)
Centroptilum triangulifer Mayfly obl XX:XO? F? D Y Y Ni,jFunk et al. (2006)
Hemiptera
Rhopalosiphum padi Aphid con XX:XO Fb?YYYYYY — —Delmotteet al. (2001)
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
On the fate of sexual traits under asexuality 5
Table 1. Continued
Species information Summary Male traits Female traits
Taxonomic
groups and
species
names
Common
name
Parthenogenesis
Sex
determination in
sexual sister
groups
Male
Female
Male
produc-
tion
‘Normal’
morphology
Courting
behaviour/
attractive-
ness to
females
Mating
behaviour
Sperm
transfer/
sper-
matophore
production
Functional
sperm
Normal
spermath-
eca; seminal
receptacles
Mate
attraction;
response to
attraction;
courtship
Normal
copulation
behaviour;
sperm/
spermatophore
uptake
Egg
fertilization
References
Hymenoptera
Nomada japonica Bee obl Haplodiploid ? D? — — — — Nc Maeta et al. (1987)
Cerapachys biroi Ant obl Haplodiploid ? D N? — — — — N Tsuji & Yamauchi (1995) and
Ravary & Jaisson (2004)
Monomorium triviale Ant obl Haplodiploid ? F? N? — — — — — Y Gotoh et al. (2012)
Mycocepurus smithii Ant A Haplodiploid ? D N? — — — — — N Himler et al. (2009) and Rabeling
et al. (2011)
Pristomyrmex punctatus (pungens) Ant obl Haplodiploid F F? Y Y YkY— —Itowet al. (1984) and Gotoh et al.
(2012)
Pyramica membranifera Ant obl Haplodiploid ? F? N? — — — — Y Ito et al. (2010) and Gotoh et al.
(2012)
Diplolepis rosae Gall wasp obl Haplodiploid F D Y Y Y N Stille & Davring (1980)
Aphytis diaspidis Parasitoid wasp AfHaplodiploid F D YfY—Y Y Y
kYY
lY N Zchori-Fein et al. (1995)
Aphytis lingnanensis Parasitoid wasp AfHaplodiploid F D YfYYYYY
kYY
lY N Argov et al. (1995) and
Zchori-Fein et al. (1995)
Aphytis mytilaspidis Parasitoid wasp AfHaplodiploid F D YfY Y Y Y N Rossler & Debach (1973)
Aphytis yanonensis Parasitoid wasp oblfHaplodiploid F? ? YfY Zchori-Fein et al. (1995, 1998) and
Burger (2009)
Encarsia formosa Parasitoid wasp oblfHaplodiploid D D YfYYN
cNY
kYmY? N? N Zchori-Fein et al. (1992), Kajita
(1993), and Hunter (1999)
Encarsia hispida Parasitoid wasp oblfHaplodiploid F? ? YfY Hunter (1999) and Giorgini et al.
(2009)
Encarsia meritoria Parasitoid wasp AfHaplodiploid F F? YfYYYYY
kY Giorgini (2001)
Encarsia perniciosi Parasitoid wasp A Haplodiploid F? D Y Y N N Stouthamer & Luck (1991)
Encarsia protransvena Parasitoid wasp oblfHaplodiploid D D YfN N N N N N Giorgini (2001)
Eretmocerus mundus Parasitoid wasp AfHaplodiploid F D Yf——Y Y Y
kY Y? N N De Barro & Hart (2001)
Asobara japonica Parasitoid wasp AfHaplodiploid F D YfYN
eYYY
g N N N Kremer et al. (2009) and Reumer
(2012)
Lysiphlebus fabarum Parasitoid wasp con Haplodiploid Fb? Y Y Y Y Y Y Belshaw et al. (1999), Sandrock
et al. (2011), and Sandrock &
Vorburger (2011)
Apoanagyrus diversicornis Parasitoid wasp AfHaplodiploid F D YfYYYYY
gN N N Pijls et al. (1996)
Diaphorencyrtus aligarhensis Parasitoid wasp oblfHaplodiploid F F YfY Y Y Y Y Meyer & Hoy (2007)
Gronotoma micromorpha Parasitoid wasp obl Haplodiploid F D Y Y Y Y Yk Y Y N Arakaki et al. (2001)
Galeopsomyia fausta Parasitoid wasp oblfHaplodiploid F D YfYYYYY
kY Y? N N Argov et al. (2000)
Neochrysocharis formosa Parasitoid wasp AfHaplodiploid D D YfY N N N N Adachi-Hagimori et al. (2011)
Pnigalio soemius Parasitoid wasp AfHaplodiploid F? ? YfY Giorgini et al. (2010)
Leptopilina clavipes Parasitoid wasp AfHaplodiploid F D YfYYYYY
gNY N
cNjPannebakker et al. (2005) and
Kraaijeveld et al. (2009)
Tetrastichus coeruleus Parasitoid wasp AfHaplodiploid F? D YfY———N N
cNN
jReumer (2012)
Venturia canescens Parasitoid wasp con? Haplodiploid F D Y Y Y Y Y Y Y Y Y NjSchneider et al. (2003)
Muscidifurax uniraptor Parasitoid wasp oblfHaplodiploid D D YfYYYNNN N
cN N Gottlieb & Zchori-Fein (2001)
Telenomus nawai Parasitoid wasp AfHaplodiploid F D YfYYY
lYlYY
l Y N Arakaki et al. (2000) and Jeong &
Stouthamer (2005)
Trichogramma brevicapillum Parasitoid wasp AfHaplodiploid F F YfYY
lYlYlYY
lYlYlY Stouthamer & Werren (1993)
Trichogramma chilonis Parasitoid wasp AfHaplodiploid F F YfYY
lYlYlYY
l—Y
lY Stouthamer et al. (1990a,b)
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
6Casper J. van der Kooi and Tanja Schwander
Table 1. Continued
Species information Summary Male traits Female traits
Taxonomic
groups and
species
names
Common
name
Parthenogenesis
Sex
determination in
sexual sister
groups
Male
Female
Male
produc-
tion
‘Normal’
morphology
Courting
behaviour/
attractive-
ness to
females
Mating
behaviour
Sperm
transfer/
sper-
matophore
production
Functional
sperm
Normal
spermath-
eca; seminal
receptacles
Mate
attraction;
response to
attraction;
courtship
Normal
copulation
behaviour;
sperm/
spermatophore
uptake
Egg
fertilization
References
Trichogramma cordubensis Parasitoid wasp oblfHaplodiploid F F YfYY
lYlYlYY
lNcYlY Silva & Stouthamer (1997)
Trichogramma deion Parasitoid wasp AfHaplodiploid F F YfYY
lYlYlYY
lYlYlY Stouthamer et al. (1990b),
Stouthamer & Luck (1993),
and Stouthamer & Kazmer
(1994)
Trichogramma embryophagum Parasitoid wasp AfHaplodiploid F? ? YfY Pinto & Stouthamer (1994)
Trichogramma kaykai Parasitoid wasp AfHaplodiploid F F YfYY
lYl—Y— — Y
lY Stouthamer & Kazmer (1994)
and Hohmann et al. (2001)
Trichogramma nr deion Parasitoid wasp AfHaplodiploid F F YfY———— — Y
lY Stouthamer & Kazmer (1994)
Trichogramma olae Parasitoid wasp oblfHaplodiploid F F YfYY
lYlYlYY
lYlYlY Stouthamer et al. (1990b)and
Grenier et al. (2002)
Trichogramma platneri Parasitoid wasp AfHaplodiploid F F YfYY
lYlYlYY
lYlYlY Stouthamer et al. (1990a,b)
Trichogramma pretosium Parasitoid wasp AfHaplodiploid F F YfYY
lYl—Y— — Y
lY Stouthamer et al. (1990b),
Stouthamer & Luck (1993),
and Stouthamer & Kazmer
(1994)
Trichogramma rhenana Parasitoid wasp AfHaplodiploid F F YfYY
lYlYlYY
lYlYlY Stouthamer & Werren (1993)
Lepidoptera
Dahlica (Solenobia)triquetrella (2n strain) Bagworm moth A ZO:ZZ; ZW:ZZ F VAR Y Y Y Y Y Y VAR Y VAR Seiler (1960, 1963)
Dahlica (Solenobia) triquetrella (4n strain) Bagworm moth obl ZO:ZZ; ZW:ZZ ? D N Y NcYN
jSeiler (1960, 1963)
Dahlica (Solenobia)lichenella Bagworm moth obl ZW:ZZ ? D N Y N Seiler & Puchta (1956)
Luffia ferchaultella Bagworm moth obl ZO:ZZ ? D N? Y Y Y Ni,jNarbel-Hofstetter (1962,
1966)
Orthoptera
Poecilimon intermedius Bushcricket obl XX:XO ? D N? YmN Y N? Lehmann et al. (2007, 2011)
Saga pedo (4n) Bushcricket obl XX:XO F? D Y Y Ym—YN
jLemonnier-Darcemont &
Darcemont (2007, 2008)
and Baur (2010)
Phasmida
Bacillus atticus Stick insect obl XX:XO F F Y Y Y Scali (2009, 2013)
Bacillus rossius Stick insect A XX:XO F F Y Y Y Y Y Scali (1968, 2009)
Carausius morosus Stick insect obl XX:XO D D Y Y — Y — N Y N Pijnacker (1964)
Timema douglasi Stick insect obl XX:XO F D Y Y Y Y Y YgNcNcY N Schwander et al. (2013)
Timema genevievae Stick insect obl XX:XO F D Y Y Y Y Y YgNcNcY N Schwander et al. (2013)
Timema monikensis Stick insect obl XX:XO F D Y Y Y Y Y YgNcNcY N Schwander et al. (2013)
Timema shepardi Stick insect obl XX:XO F D Y Y Y Y Y YgNcYYNSchwanderet al. (2013)
Timema tahoe Stick insect obl XX:XO ? D N? NcNcY N Schwander et al. (2013)
Psocoptera
Caecilius aurantiacus Psocid A XX:XO ? D N? N Mockford (1971)
Bertkauia lucifuga Psocid obl XX:XO F D Y Y Y Y NcN Mockford (1971)
Liposcelis bostrychophila Psocid obl XX:XO? F? ? Y Y Mockford & Krushelnycky
(2008) and Wang et al.
(2008)
Peripsocus quadrifasciatus Psocid A XX:XO ? D N? N Mockford (1971)
Psocus bipunctatus Psocid A XX:XO ? D N? N N Mockford (1971)
Thysanoptera
Franklinothrips vespiformis Thrips oblfHaplodiploid F D YfY—YY Y
kY Y N Arakaki et al. (2001)
Anaphothrips obscurus Thrips obl Haplodiploid F? ? Y Y Mirab-Balou & Chen (2010)
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On the fate of sexual traits under asexuality 7
Table 1. Continued
Species information Summary Male traits Female traits
Taxonomic
groups and
species
names
Common
name
Parthenogenesis
Sex
determination in
sexual sister
groups
Male
Female
Male
produc-
tion
‘Normal’
morphology
Courting
behaviour/
attractive-
ness to
females
Mating
behaviour
Sperm
transfer/
sper-
matophore
production
Functional
sperm
Normal
spermath-
eca; seminal
receptacles
Mate
attraction;
response to
attraction;
courtship
Normal
copulation
behaviour;
sperm/
spermatophore
uptake
Egg
fertilization
References
Heliothrips haemorrhoidalis Thrips obl Haplodiploid F? D Y Y N N Mound (1976) and Del Bene
et al. (1998)
Hercinothrips femoralis Thrips oblfHaplodiploid F D YfY—Y Y Y
kNc Y N Moritz (1989) and Kumm &
Moritz (2008)
Parthenothrips dracaenae Thrips obl Haplodiploid F D Y Y YkNc N Lewis (1973) and Kumm
(2002)
Thrips nigropilosus Thrips A Haplodiploid ? D NcN Nakao & Yabu (1998)
MOLLUSCA
Gastropoda
Potamopyrgus antipodarum (jenkinsi) (3n) Snail A UnknownaFD Y Y Y
kNcY Y Patil (1958) cited in Bell
(1982), Neiman & Lively
(2005), Nelson & Neiman
(2011), and Neiman et al.
(2012)
Melanoides tuberculata (5-6n) Snail A Unknown D ? Y Y N Jacob (1954, 1957)
Melanoides lineatus (4n) Snail A Unknown D ? Y Y N Jacob (1954, 1957)
Parthenogenesis: A, asexual lineages in species with both asexual and sexual strains; obl: obligately asexual species; con: contagious parthenogenesis (functional males are expected given their reproductive success in matings with sexual
females). Lineages are diploid unless otherwise specified (2n: diploid, 3n: triploid, 4n: tetraploid); species and genera names in parentheses indicate synonyms. The combined evidence for different male and female traits is summarized as:
D (decayed) or F (functional). Y (yes): trait is fully expressed and functional; N (no): functionality reduced or lacking; — : no information available for the trait; 0: trait does not exist for this species; ?: inference uncertain; VAR (variable):
functional in some, non-functional in other strains; see footnotes and text for details.
aDiplo-diploid sex determination but no known sex chromosomes.
bMales most likely do not produce sperm at all.
cTraits are still present but reduced or altered; for example asexually produced males are less attractive than sexual males, or courting is rarer or reduced in comparison to sexual males; sperm-storage organs are present but smaller/altered
shape relative to sexual strains.
dSome ‘males’ have intersexual characteristics.
eNo courting or mating behaviour in these species; spermatophores are deposited and left unattended by males and picked up (or not) by females.
fParthenogenesis is endosymbiont induced; production of males after antibiotic or heat treatment, usually also at a low rate in natural/untreated populations.
gSperm from asexually produced males is functional in crosses with sexual females, but fertilization efficiency is reduced in comparison to sexual males - notice that in these cases it is not possible to disentangle the effect of asexuality
from an effect of incompatibility between diverged populations and species/cryptic female choice.
hReported males are probably from sexual strains.
iFertilized eggs: low viability and intersex development.
jVery low rate of fertilization (sometimes only paternal gene leakage).
kSperm motile and appeared functional in assays, but functionality was not confirmed via crosses with sexual females.
lFunctionality of the trait is not directly documented in studies but inferred, given the successful fertilization of sexual females/reversibility of asexuality.
mTrait state uncertain because no comparison with sexual relatives available.
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
8Casper J. van der Kooi and Tanja Schwander
endosymbionts also lay haploid eggs, but these eggs become
diploid via gamete duplication and develop into females
(Stouthamer & Kazmer, 1994). If such infected asexual
females are cured from their endosymbionts (for example via
antibiotic treatment) they produce sons instead of daughters,
given that their haploid eggs remain haploid and develop
into males. For these species it is thus possible to obtain
large numbers of males from all-female asexual lineages (e.g.
Stouthamer et al., 1990a; Pannebakker et al., 2005; Kremer
et al., 2009).
V. FATE OF MALE-SPECIFIC TRAITS IN
ASEXUAL LINEAGES
For asexual lineages that do not produce any males (and for
which male production cannot be induced by antibiotic
treatment), it is impossible to distinguish whether male
phenotypes are simply not expressed, or whether the
pathways underlying male development have decayed. In
other words, the functionality of male sexual traits can only
be investigated in the subset of lineages that maintain the
developmental pathways leading to the differentiation of
males.
Among the 93 asexual lineages for which any information
on sexual traits (male or female expressed) is available, at
least 74 are able to produce males even though they are most
likely obligately asexual (Table 1). Males in a minority of
these lineages (3 out of the 74) regularly mate with females
of related sexual lines and thereby generate new asexual
lineages (‘contagious parthenogenesis’; Delmotte et al., 2001;
Paland, Colbourne & Lynch, 2005; Sandrock, Schirrmeister
& Vorburger, 2011). In these cases, the maintenance of
male functionality is expected, given the mating success of
asexually produced males. For the remaining 71 lineages, the
absence of mating opportunities for asexually produced males
should result in relaxed selection on male traits, which may
then decay as a consequence of drift. In these lineages, males
are considered to be developmental accidents, whereby their
production occurs too rarely to be associated with measurable
costs, at least in species with high reproductive output
(Neiman et al., 2012). Given that trait decay as a consequence
of drift is expected to proceed slowly, relatively little decay
would be expected for male-specific traits in asexuals overall,
and more extensive decay in old as compared to young
asexual lineages. Consistent with these predictions, studies
report little or no evidence for morphological decay of males
in the lineages known to produce accidental males, with
functional decay of males in only 13 lineages (Table 1).
Although the unknown age of most asexual lineages makes
it impossible to assess whether the 13 lineages with decayed
male traits are relatively old compared to the lineages with
functional males, two lines of evidence are suggestive that
this may be the case. First, two of the species with reported
decay of male traits are oribatid mites, a group hypothesized
to have been asexual for 100 million years (Maraun et al.,
2003; Domes et al., 2007; Heethoff et al., 2007). Second, for
11 of the 13 lineages with decayed male traits, there is also
information available on the functionality of female sexual
traits, which are strongly reduced in nine cases. Additional
information for more lineages on the time passed since the
inception of asexuality would provide insights into the time
frame required for the neutral decay of male traits.
The male traits to decay first under asexuality appear to
be largely linked to fertility and sperm production. Courtship
behaviours and morphological traits generally remain fully
functional and equivalent to behaviours and trait values in
related sexual males. Thus, in 11 of the 13 species with
evidence for decay of male traits, males produce immotile
sperm or have otherwise dysfunctional spermatogenesis
(Table 1). Similarly, in at least eight asexual lineages where
asexually produced males appear fully functional, these males
are characterized by lower fertilization efficiency of eggs from
sexual females when compared to sexual males. Although this
may also stem from sexualasexual hybrid incompatibilities
or cryptic female choice (see Schwander et al., 2013), this
pattern is consistent with traits linked to spermatogenesis
being the first to decay.
A rapid decay of sperm functionality relative to other
male traits may stem from two non-exclusive processes.
First, the genetic architecture underlying sperm functionality
traits may be such that there are many possible targets
for loss of function mutations. Indeed as noted 40 years
ago, mutations causing male sterility in Drosophila melanogaster
appear to be 1015% more frequent than mutations causing
lethality (Lindsley & Lifschytz, 1972). Second, gene networks
underlying spermatogenesis may involve more male-specific
elements without pleiotropic effects in females than male
morphological and behavioural traits. Genes expressed in
testis of Drosophila melanogaster and Anopheles gambiae males are
among the most highly tissue specific (Chintapalli, Wang &
Dow, 2007; Baker et al., 2011) suggesting that their alteration
may indeed be devoid of consequences in females.
The mechanisms underlying accidental male production
by asexual females depend on the sex-determination system
present in the sexual ancestors. In the species where
parthenogenesis is induced by endosymbiotic bacteria, male
development has been hypothesized to occur in individuals
with low bacterial titres, or in lineages where the efficiency of
host reproductive manipulation by the bacteria is lower than
100% (e.g. Huigens & Stouthamer, 2003; Koivisto & Braig,
2003; Reumer, van Alphen & Kraaijeveld, 2012; notice
that eggs unaffected by bacterial manipulation will develop
into males given the haplodiploid sex-determination system
in these species). In asexuals deriving from species with
XX:XO sex determination (females have two, males only
one X chromosome), males can develop as a consequence of
accidental sex chromosome losses via non-disjunction (Scali,
1968, 2013; Baur, 2010). Such sex chromosome losses are less
likely to generate functional males in species with XX:XY
sex determination (and functional genes on the Y), and
indeed there are no known instances of male production by
asexual lineages deriving from sexual ancestors characterized
by this sex-determination system (though XY chromosomal
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
On the fate of sexual traits under asexuality 9
sex determination, with the gene content on the Y unknown,
remains possible in several cases where the sex-determination
system in sexual sister groups is uncertain; Table 1).
There are only a few documented cases of accidental
male production by asexual females in taxa with female
heterogamety (females are ZW or ZO, males ZZ; Table 1).
In many of these species, especially in different asexual
bagworm moths, reproduction occurs via a meiotic type of
parthenogenesis, where two of the four meiotic products
fuse to re-establish the maternal ploidy levels (reviewed in
Suomalainen, Saura & Lokki, 1987). This fusion does not
occur at random but is always between the two central nuclei,
which results in offspring having the same chromosome
complement as their mother (Suomalainen et al., 1987). Thus,
this mechanism also maintains the ZW (or ZO) chromosomal
constitution, leading to the production of daughters. It seems
plausible that errors during meiosis could rarely lead to
the fusion of two different nuclei, which would generate ZZ
individuals that would develop into males (Suomalainen et al.,
1987). However, the karyotype of accidental males in these
species has not been investigated thus far, such that male
development may also stem from other processes.
Given the mechanisms underlying accidental male
production in species with XX:XO sex determination, the
maintenance of male functionality in many asexual lineages
is somewhat paradoxical. In asexual females, all loci occur
exclusively in a diploid (or polyploid) state such that recessive
deleterious alleles are constantly masked and could therefore
accumulate. In asexually produced males however, recessive
alleles present on the X chromosome would be expressed
in diploid asexuals, given the hemizygous state of this
chromosome in males assuming that there was enough
time for the build-up of a recessive load. It remains possible
that the few documented male individuals represent the tip of
an iceberg of XO eggs, most of which would die in the course
of their development due to recessive deleterious mutations
on the X. However, this would require chromosomal non-
disjunctions to be quite frequent, entailing significant fertility
costs for females. Interesting questions for future studies are
thus whether gene conversion or some other mechanism can
reduce the accumulation of recessive deleterious alleles in
asexuals, and if some of the dysfunctional traits in asexually
produced males stem from the expression of recessive alleles.
In comparison to species with XX:XO sex determination,
male phenotypes in haplodiploid groups with endosymbiont-
induced parthenogenesis should be less affected by the
expression of recessive alleles. This is because asexual females
are fully homozygous, given their development from haploid
eggs that undergo gamete duplication. Perhaps this is the
main reason for why particularly many such asexual species
are known to produce males and why these males typically
show a complete lack of decay (Table 1).
Overall the ubiquitous maintenance of male traits across
the majority of asexual lineages would be best explained
by neutral decay requiring millions of years to result
in significant phenotypic effects, a time frame rarely
reached by asexual lineages (Schurko, Neiman & Logsdon,
2009). In addition, male developmental and physiological
pathways may consist almost exclusively of components with
pleiotropic effects in both sexes, which would prevent these
elements from degenerating. When by some rare accident
the male developmental pathway is triggered, it would
therefore still generate functional males. Alternatively, the
development of functional males may indicate that lineages
presumed to be asexual have some low level of cryptic
sex. However, although formally demonstrating the lack of
sexual reproduction in a lineage is challenging (Schurko
et al., 2009), this explanation is difficult to reconcile with the
decay of female sexual traits reported in the vast majority of
asexual lineages, including most cases with functional males
(see Section VI).
VI. FATE OF FEMALE SEXUAL TRAITS IN
ASEXUALS
In contrast to the maintained male traits, female-linked sexual
traits show evidence for decay in the majority (82%) of asexual
lineages. Among the 73 asexual lineages for which a range of
female traits were investigated, a significant reduction of at
least one, but typically several, sexual traits was reported in 60
cases (Table 1). Such broad-scale trait decay should severely
impede reversals to classical forms of sexual reproduction.
Sexual trait decay could thus provide a positive line of
evidence (sensu Schurko et al., 2009; Birky, 2010) for obligate
asexuality in a lineage, provided that decayed traits are fixed
rather than phenotypically plastic and that the sample of
analyzed asexual females allows excluding the occurrence of
extremely rare females (i.e. those occurring at frequencies
similar to the frequency of rare males among asexual females)
with functional sexual traits.
Among the 60 lineages with female sexual trait decay, the
ability to use sperm for egg fertilization is completely lacking
or at least strongly reduced in all 38 species where this
trait was investigated. Thus, for 31 out of these 38 lineages
(Table 1), sperm was not integrated into eggs and there was no
evidence for any paternal genetic contribution to offspring. In
the seven remaining species, there is occasional fertilization of
small egg fractions, whereby in at least two cases, individuals
developing from fertilized eggs are developmentally instable
and often display intersexual traits (Table 1). This pattern
strongly suggests selective mechanisms driving the trait
shift. Egg fertilization could be very costly for asexuals,
for example if ploidy elevation reduces egg or offspring
viability, as suggested by developmental abnormalities in
the species where partial fertilization of asexual eggs occurs.
Alternatively, this trait could be linked to the origin of
asexuality per se. For example, gene flow from sexual
strains could prevent the initial establishment of a new
asexual lineage lacking strong barriers to paternal genetic
contributions (Lynch, 1984). Such a barrier is described
in the asexual bushcricket Saga pedo: eggs have a reduced
number of micropyles (pores in the ovum membrane
through which sperm enter) as compared to sexual
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
10 Casper J. van der Kooi and Tanja Schwander
relatives, limiting the chances of eggsperm interactions
(S¨
anger & Helfert, 1994). Mutations allowing for asexual
embryo development may also entail correlated changes
constraining eggsperm interactions. This could explain
why fertilization ability is only maintained in hymenopteran
species with endosymbiont-induced asexuality (Table 1),
where transitions to asexuality do not involve modifications
of egg types laid (both virgin sexual and asexual females lay
haploid eggs). In this sense, the absence of egg fertilization
in asexuals may not always indicate decay of a sexual trait.
Further research in incipient asexual lineages and their
interactions with sexual populations may provide insights
into the evolutionary process underlying the loss of egg
fertilization ability in asexuals.
Parallel losses also occur for traits involved in mate
location or copulation propensity, consistent with the idea of
selection acting to reduce such traits to diminish costs linked
to exposure to predators and diseases. The best evidence
for selection-driven decay stems from traits underlying
mate location and attraction, given that these traits have
regressed in parallel in groups using different signalling
systems (notably based on olfactory or auditory signals)
and independently of whether females are the emitting
or responding sex. For example in sexual bushcricket
species, females are the responding sex and are attracted by
males with songs (Gwynne, 2001). The asexual bushcricket
P. intermedius has completely lost phonotaxis within fewer
than 200000 years and displays a morphological reduction
of hearing-related structures (Lehmann, Strauss & Lakes-
Harlan, 2007; Lehmann et al., 2011).
Among insect species using chemical communication,
however, females are typically the signalling rather than
the responding sex and emit pheromones and other olfactory
cues to attract males (Greenfield, 2002). Here, females in
several asexual stick insect species produce either no cues
or cues that are not attractive to males (Schwander et al.,
2013). A lack of pheromones eliciting male courtship or a
lack of female sexual behaviour is also reported in species
with endosymbiont-induced parthenogenesis (e.g. Pijls, Van
Steenbergen & van Alphen, 1996; Silva & Stouthamer, 1997;
Pannebakker et al., 2005; Kremer et al., 2009). An additional
line of evidence supporting selective rather than neutral
regression of mate-attraction traits stems from asexual stick
insect lineages, where the extent of attractivity loss depends
less on the age of the asexuals than on distribution patterns;
young asexuals overlapping with their sexual counterparts
display more extreme decay than old asexuals isolated from
sexual species (Schwander et al., 2013). Although Potamopyrgus
antipodarum snails, where females appear to play a passive role
in mate finding and copulation, may represent an exception
to this pattern (Nelson & Neiman, 2011), these parallel
and rapid losses of different female traits involved in mate
attraction and mating suggest that selective mechanisms,
rather than drift, are driving trait changes.
Similar to the preserved male traits, female sexual traits
not exposed to selection also tend to be maintained, even in
species with extensive trait decay overall. For example in the
asexual bushcricket with reduced phonotaxis and hearing
organs, no decline in female mating behaviour has been
observed when asexual females are confined with males of
related sexual species (Lehmann et al., 2011). Since without
phonotaxis, asexual females are not attracted to males and
will therefore typically not encounter them under natural
conditions, copulation behaviour in asexual females is no
longer expressed and could therefore only regress via drift.
Female sperm-storage organs are also often maintained
and hence appear to be associated with little or no costs.
Only two studies report a decay of the ability to store
sperm in asexual females (Gottlieb & Zchori-Fein, 2001;
Kraaijeveld et al., 2009) whereas in most cases, spermathecae
in asexuals display only altered shapes relative to sexuals or
more variability, indicating reduced developmental stability
of the organ (Table 1). Both patterns are consistent with trait
decay as a consequence of relaxed selection, but it is difficult
to see why a somewhat altered shape would reduce possible
costs associated with spermatheca differentiation.
Fully maintained female functionality was documented
in only 13 out of the 73 asexual lineages for which
a range of female traits were investigated (18%). It is
notable that 11 of these 13 species are hymenopterans
with endosymbiont-induced parthenogenesis, 10 from the
same genus (Trichogramma) of parasitoid wasps (Table 1).
In this genus parthenogenesis is even revertible, as stable
sexual populations can be derived from asexual lines by
curing the females of their endosymbionts (Stouthamer et al.,
1990a,b). The lack of sexual trait decay in these species may
stem from infections being very recent and/or from ongoing
gene flow between sexual and asexual lines. Consistent with
these explanations, allele sharing in natural populations with
alternative reproductive modes, as well as paternal genome
leakage into asexual lineages in laboratory crosses between
asexual females and sexual males, is documented in several
Trichogramma species (Stouthamer et al., 1990a,b; Stouthamer
& Luck, 1993; Stouthamer & Kazmer, 1994). The two
remaining asexual lineages with maintained female sexual
traits are stick insects from the genus Bacillus, which may be
facultative parthenogens (Scali, 2009).
In addition to the typical female-expressed sexual traits,
there are certain taxon-specific traits that have also regressed
after transitions to asexual reproduction. However, given the
uniqueness of these traits, processes underlying their decay
cannot be inferred from comparative approaches. One such
taxon-specific trait is the use of different hosts for male and
female offspring by certain groups of parasitoid wasps (the use
of different hosts for the production of sons versus daughters
is believed to originate from sex-specific optimal resource
conditions and developmental requirements; Hunter, 1999).
Asexual species in these groups thus only lay eggs into
the female-specific host and three asexual hymenopteran
species in the Aphelinidae family have lost the behaviour of
switching hosts for male offspring (Hunter, 1999; Zchori-Fein
et al., 2001; Kenyon & Hunter, 2007). Since the behaviour
to search and find hosts for male larvae is not expressed
in asexual females, the trait would have regressed via drift,
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
On the fate of sexual traits under asexuality 11
in contrast to the general pattern that extensive sexual trait
changes would stem from selective processes. However, the
lack of male host usage by asexual Aphelinidae females is
more likely due to changes in the hosts than in the parasitoids;
co-evolutionary dynamics of hosts avoiding detection by
parasitoids and parasitoids recognizing volatile and other
cues emitted by the hosts is expected to drive continuous
change in both hosts and parasitoids (Vinson, 1975). Thus,
asexual wasps would be able to identify ancestral male-host
cues present prior to the transition to asexuality, but not the
contemporary version of such cues.
VII. GENETIC ARCHITECTURE OF DECAYED
TRAITS
An open question remaining is the genetic architecture
underlying trait decay. Thus it is largely unknown whether
trait decay typically proceeds by the accumulation of
mutations with small phenotypic effects, or in large
increments, for example as a consequence of major effect
mutations in regulatory sequences or highly connected
elements (Jeffery, 2001, 2009; Lahti et al., 2009). Thus far,
data on sexual trait decay point to the latter. These data stem
from three studies in hymenopterans with endosymbiont-
induced asexuality. In these species, the genetic architecture
of decayed sexual traits can be investigated by introgressing
genes from asexual into sexual lines, taking advantage of sons
produced by asexual females cured of their endosymbionts
(Pannebakker et al., 2004; Jeong & Stouthamer, 2005; Russell
& Stouthamer, 2011).
The first study to investigate the genetic basis of trait
decay focused on the fertility of asexually produced males
(Pannebakker et al., 2004), whereby ‘fertility’ was assessed
from offspring sex ratios produced by sexual females (low
fertility would be indicated by male-biased sex ratios, since
successfully fertilized eggs develop into females). A single,
major effect locus affecting male fertility was identified via an
elegant mapping approach, consistent with a simple genetic
architecture underlying trait decay (Pannebakker et al., 2004).
However, hymenopteran females might adjust their offspring
sex ratios according to the quality of their mates, producing
more fertilized (female) eggs when mated with a high-quality
male (e.g. West & Sheldon, 2002). Thus, given that male
fertilization ability in this study was assessed indirectly from
offspring sex ratios in crosses with females of a sexual strain,
it is difficult to exclude that the uncovered locus is associated
with male attractiveness to females rather than with male
fertility.
The two remaining studies focused on egg fertilization
ability of females and found evidence for a single locus
underlying the loss of egg fertilization in asexuals, recessive
in one and dominant in the other study, with additional
minor-effect modifiers (Jeong & Stouthamer, 2005; Russell
& Stouthamer, 2011). Similar to the earlier study, these
patterns would also indicate a simple genetic architecture
of trait decay. However, as noted above, the lack of egg
fertilization ability in asexuals may be linked to the origin
of asexuality, rather than indicating sexual decay, such that
generalizations for the genetic architecture of decayed traits
are difficult.
The current evidence thus points to sexual trait decay
stemming from very few mutations with relatively strong
phenotypic effects. While generalizations from these studies
for trait decay may be difficult, they provide guidelines
for future studies investigating the genetic architecture
of regressed traits. Additional such studies are thus
highly warranted, especially for well-characterized traits
clearly stemming from the loss of sexual reproduction, in
hymenopterans as well as in other taxa. Given the fertility
of asexually produced males in many asexual lineages, such
approaches should be feasible even with only a handful
of males available. Insights from such studies may notably
inform on the influence of trait complexity on its rate of decay.
A complex trait consisting of many components may display
signatures of decay more rapidly than a simple trait because
more targets are available for mutations with phenotypic
effects. Alternatively, the opposite may be true if modifying
one element is enough (Jeffery, 2001). Finally, insights into
the genetic basis of trait decay may also shed light on loci
underlying trait variation among sexual species.
VIII. CONCLUSIONS
(1) Research on trait decay is important because it
provides insights into the selective pressures generating and
maintaining traits. Given the energy required to produce
and maintain most characters, useless features may often be
a disadvantage and their reduction should be favoured by
natural selection (Regal, 1977).
(2) The combined evidence from studies of sexual traits
in 93 independently derived asexual lineages suggests that
trait decay typically only occurs if driven by selective
processes. Traits expected to be under relaxed selection
and decay via neutral mutation accumulation were generally
fully functional, or displayed only minor shifts (not affecting
functionality) since the abandonment of a sexual lifecycle.
(3) The ubiquitous maintenance of male traits across the
majority of asexual species would be best explained by neutral
decay requiring millions of years to result in significant
phenotypic effects, a time frame rarely reached by asexual
lineages (Schurko et al., 2009), or by male developmental
and physiological pathways consisting almost exclusively
of components with pleiotropic effects in both sexes. The
maintenance of male developmental pathways reveals that
major developmental pathways can remain quiescent and
functional over extended time periods.
(4) In contrast to the maintained male traits, sexual traits
in asexual females display large-scale shifts relative to sexual
females, often indicating decay. Traits decayed in parallel
across many asexual lineages are involved in mate attraction
or location, as well as copulation behaviours, as expected
given the potentially considerable costs associated with the
Biological Reviews (2014) 000– 000 ©2014 The Authors. Biological Reviews ©2014 Cambridge Philosophical Society
12 Casper J. van der Kooi and Tanja Schwander
expression of these traits. Asexual females also consistently
lack the ability to fertilize eggs or include paternal genetic
contributions in offspring, but this pattern may be linked
to the origin of asexuality rather than being a case of trait
decay.
(5) More generally, we expect that the majority of trait
losses stem from selection rather than the relaxation thereof,
and that losses typically occur in large increments rather
than by the accumulation of small steps. There would thus
be few instances of intermediate situations with traits in the
process of decay, such that in modern taxa only reduced trait
values are observed, for which further reduction provides no
additional fitness benefits.
IX. ACKNOWLEDGEMENTS
We thank an anonymous reviewer for insightful comments on
the manuscript, Jelmer Elzinga and Jens Bast for providing
information and references on different asexual groups and
Laurent Bes for drawing Fig. 1. This research was funded by
grants from the NWO and FNS to T.S.
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... Adaptations that were once important for survival that subsequently become useless or impose 25 new fitness costs tend to decay over time in a process known as vestigialisation [1][2][3]. Many 26 examples of this phenomenon can be seen throughout evolutionary history, including the loss of 27 limbs in snakes [4], eye structures in cave-dwelling fish [5], and wings in many insect species 28 [6]. ...
... Mating behaviours are themselves associated with 42 numerous costs [9,10]. Accordingly, vestigialisation of mating-related traits in asexual lineages 43 -including those involved in mate choice -is expected, particularly in a scenario where such 44 behaviours and their maintenance are costly [3,11,12]. Alternatively, these traits may be 45 selectively neutral or maintained by selection in asexuals, but only in a context where the costs 46 . ...
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Once-useful traits that no longer contribute to fitness tend to decay over time. We address whether the expression of mating-related traits that increase the fitness of sexually reproducing individuals but are likely less useful or even costly to asexual counterparts seems to exhibit decay in the latter. Potamopyrgus antipodarum is a New Zealand freshwater snail characterized by repeated transitions from sexual to asexual reproduction. The frequent coexistence of sexual and asexual lineages makes P. antipodarum an excellent model for the study of mating-related trait loss. We used a mating choice assay including sexual and asexual P. antipodarum females and conspecific (presumed better choice) vs. heterospecific (presumed worse choice) males to evaluate the loss of behavioural traits related to sexual reproduction. We found that sexual females engaged in mating behaviours with conspecific mating partners more frequently and for a greater duration than with heterospecific mating partners, while asexual females seemed to lack the ability to make a choice. These results suggest that selection acting to maintain mate choice in asexual P. antipodarum is weak or ineffective relative to sexual females and that asexual reproduction likely contributes to the evolutionary decay of behavioural traits in this system.
... In asexual life cycles, sex pheromone production is useless and can be considered a neutral or maladaptive trait depending on the amount of energy cost required for their expression, as we have pointed out previously . It has been suggested that a formerly adaptive trait can be reduced when that trait is neutral or maladaptive in the new selective environment (van der Kooi & Schwander, 2014;Lahti et al., 2009;Lynch, 1984). In animal parthenogens, the decay of female sexual traits has been widely reported (van der Kooi & Schwander, 2014). ...
... It has been suggested that a formerly adaptive trait can be reduced when that trait is neutral or maladaptive in the new selective environment (van der Kooi & Schwander, 2014;Lahti et al., 2009;Lynch, 1984). In animal parthenogens, the decay of female sexual traits has been widely reported (van der Kooi & Schwander, 2014). At present, since it is unclear whether the suppression/loss of sex pheromone production occurred before or after the evolution of parthenogens, we cannot conclude whether the loss of sexual traits represents the direct origin of parthenogens or the regressive evolution of a useless trait under asexuality. ...
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Geographic parthenogenesis, a phenomenon where parthenogens and their close sexual relatives inhabit distinct geographic areas, has been considered an interesting topic in evolutionary biology. Reports of geographic parthenogenesis from land and freshwater are numerous, however, this occurrence has been rarely reported from the sea. Brown algae are mostly marine and are thought to include numerous obligate parthenogens; still, little is known about the distribution, origin, and evolution of parthenogens in this group. Here we report a novel pattern of geographic parthenogenesis in the isogamous brown alga Scytosiphon lomentaria. Sex ratio investigation demonstrated that, in Japan, sexual populations grew in the coast along warm ocean currents, whereas female-dominant parthenogenetic populations grew mainly in the coast along a cold ocean current. In the two localities where sexual and parthenogenetic populations were parapatric, parthenogens grew in more wave-exposed areas than sexuals. Population genetic and phylogenetic analyses, including those based on genome-wide single nucleotide polymorphism data, indicated that parthenogens have initially evolved at least twice and subsequent hybridizations between the parthenogens and sexuals have generated multiple new parthenogenetic lineages. The origin of the initial parthenogens is not clear, except that it would not be inter-species hybridization. Interestingly, we found that the production of sex pheromones, which attract male gametes, has been independently lost in the initial two parthenogenetic lineages. This parallel loss of the sexual trait may represent the direct origin of parthenogens, or the regressive evolution of a useless trait under asexuality.
... Females in asexual lineages usually show a certain level of reduced function of sexual traits, though these are often traits not related to copulation itself, rather to mate location, attraction and fertilization of the eggs [100,101]. In Thysanoptera, however, the reduced size (Parthenothrips dracaenae; [102]) or complete loss (Heliothrips haemorrhoidalis; [103]) of the spermatheca is also known. ...
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... However, there is evidence that more complex differences exist between the selective pressures acting on sexual and asexual populations. van der Kooi & Schwander [29] reviewed the decay of sexual traits after the evolution of asexuality in animals and showed that male traits, which are presumably under relaxed purifying selection, do not decay as quickly as sexual female traits (such as ones required for mate finding), suggesting that the latter are costly and are thus actively selected against. The changes in meiosis involved in the transition to asexuality also lead to convergent evolution at the level of gene sequences and expression, indicating a further role for selection [16,17]. ...
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... This difficulty reflects our assumption of one mutation arising at a time, i.e., a mutant cannot simultaneously change both its mode of reproduction and the size of its progeny. We consider this a potential real feature in many biological systems rather than an artificial constraint imposed by our modelling choices; transitions to asexuality are indeed often difficult when the rest of the life cycle has a past of being selected to perform well under sexual rather than asexual reproduction [49][50][51]. ...
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... M. triviale is reported from East Asia, encompassing Japan, South Korea and mainland China [14]. Neither males nor inseminated females have been found to date; this has been referred to in several studies [1,4,[17][18][19][20][21][22][23]. Surprisingly, however, direct evidence of thelytoky is lacking. ...
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We report comprehensive evidence for obligatory thelytokous parthenogenesis in an ant Monomorium triviale . This species is characterized by distinct queen–worker dimorphism with strict reproductive division of labor: queens produce both workers and new queens without mating, whereas workers are completely sterile. We collected 333 nests of this species from 14 localities and three laboratory-reared populations in Japan. All wild queens dissected had no sperm in their spermathecae. Laboratory observation confirmed that virgin queens produced workers without mating. Furthermore, microsatellite genotyping showed identical heterozygous genotypes between mothers and their respective daughters, suggesting an extremely low probability of sexual reproduction. Microbial analysis detected no bacterial genera that are known to induce thelytokous parthenogenesis in Hymenoptera. Finally, the lack of variation in partial sequences of mitochondrial DNA among individuals sampled from across Japan suggests recent rapid spread or selective sweep. M . triviale would be a promising model system of superorganism-like adaptation through comparative analysis with well-studied sexual congeners, including the pharaoh ant M . pharaonis .
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In facultatively parthenogenetic populations, the prevalence of sexual reproduction depends on whether females mate and therefore produce sons and daughters or avoid mating and produce daughters only. The relative advantage of mating in such species may depend on a female’s own reproductive origin (i.e., development from a fertilised or unfertilised egg) if parthenogenesis reduces heterozygosity similarly to sexual inbreeding, or if it inhibits mating, sperm storage or fertilisation. But effects of reproductive origin on development and performance are poorly understood. Using the facultatively parthenogenetic stick insect, Extatosoma tiaratum, we quantified morphology, mating probability, and reproductive success in mated versus unmated females of sexual versus automictic (parthenogenetic) origin. We found strong evidence that increased homozygosity negatively impacted some traits in parthenogenetically produced females: compared to sexually produced females, parthenogenetically produced females were smaller and more prone to deformities in vestigial wings, but not more prone to fluctuating asymmetry in their legs. Parthenogenetically produced females received fewer mating attempts and avoided mating more often than sexually produced females. Yet, contrary to the expectation that sex should rescue parthenogenetic lineages from the detrimental effects of increased homozygosity, parthenogenetically produced females gained no net reproductive benefit from mating, suggesting that physiological constraints limit fitness returns of sexual reproduction for these females. Our findings indicate that advantages of mating in this species depend on female reproductive origin. These results could help to explain spatial distributions of sex in facultatively parthenogenetic animals and evolutionary transitions to obligate asexuality.
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Chapter
Theoretical discussion of the role of natural selection in shaping behavioral variation in different habitats has been an integral part of the study of animal behavior since the late 19th century. Herbert Spencer (1888) was among the first to argue that migrating populations that fail to adjust to environmental circumstances “are the first to disappear.” A common rationale for comparing populations or related species is the desire to identify behavioral differences that correspond with habitat properties providing different patterns of selection (Tuomi 1981, Riechert 1993, this volume). Behavioral similarities are often ignored or are treated as less interesting because the thrust of the research program emphasizes behavioral differences as an empirical test of the theory of natural selection. Nevertheless, these similarities can be as revealing of evolutionary process as are differences when they reflect behavioral convergence or slow disintegration of behavior under relaxed selection (Coss and Goldthwaite 1995). When populations invade novel habitats, they not only experience new selective regimes; they can also experience relaxed selection on specific behavioral phenotypes. This is particularly common when the new habitat is missing a class of predators that was abundant in the ancestral habitat (e.g., Curio 1975, Pressley 1981). Under relaxed selection, characters may disintegrate, presumably because mutations that result in loss of the phenotype are not at a selective disadvantage. Disintegration is not always observed, however. Instead, behavioral characters are sometimes retained for long periods of time after selection has been relaxed (Coss 1991b, Kaneshiro 1989). Inferring relaxed selection requires that the history of the contrasted populations be relatively well known. Both ancestral selective regimes and behavioral characters must be known if character polarity is to be established. Character polarity must be established to distinguish disintegration from parallel evolution of novel behavior patterns. This often is a problem in population contrasts because differentiation is usually too recent to have resulted in the evolution of enough derived characters for the use of standard cladistic methods of phylogenetic reconstruction, although recent advances in statistical and molecular techniques are promising (Foster 1994, Foster and Cameron 1996). Instead, inference of character polarity has typically relied on geological evidence and comparison with closely related species.
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Sampling of arthropods in ground and woody vegetation habitats in highland areas on the islands of Hawaii and Maui revealed six species of psocids of the genus Liposcelis. Three are new and are here described. L. maunakea sp. n. and L. volcanorum sp. n. are closely related and form a small species complex together with L. nasus Sommerman and L. deltachi Sommerman from southwestern United States and northern Mexico. A key to the species of this complex is included. The third new species, L. kipukae sp. n., is a member of group II-C with only 5 ommatidia in the eye. A key to the known species of group II-C with fewer than 7 ommatidia in the eye is included. First Hawaiian records are presented for L. bostrychophila Badonnel, L. deltachi, and L. rufa Broadhead. The first known males of L. bostrychophila are reported and described. This species is very widespread, but generally parthenogenetic.
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The thelytokous wasp Encarsia formosa Gahan Is widely used as an agent for biological control of the greenhouse whitefly Trialeurodes vaporariorum (West-Wood) In greenhouses in central and northern Europe (Van Lenteren And Woets, 1988). The mechanisms of male appearance in this parasitoid have not been fully explained (Kajita, 1989). Some authors stated that E. formosa males are hyperparasitoids (Gerling, 1966; Flanders, 1967), while others reported that the males develop as primary parasitoids (Vet And Van Lenteren, 1981). In addition, it is almost universally believed that low greenhouse temperatures precede the occurrence of males in E. formosa (Speyer, 1927). However, it has been known that high temperatures also induce the occurrence of males in several parasitoid species (Flanders, 1965; Gordh And Lacey, 1976). More recently, Stouthamer Et al. (1990) showed that thelytokous Trichogramma species can be rendered arrhenotokous by exposure to high temperatures or certain antibiotics. This paper reports that E. formosa females exposed to high temperatures or certain antibiotics can produce male offspring, which develop as primary parasitoids of the greenhouse whitefly. © 1993, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.
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Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed by viability selection. Many secondary sexual traits may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples come from species that use acoustic or olfactory mating signals, and relatively few cases of visual signal exploitation can be substantiated. Because males are usually the signaling sex, they are more at risk from predators or parasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to male signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern of female odor production. Exploitation of such sex pheromones is relatively rare. We discuss reasons for the reversal in sex roles in these species and its implications for signal exploitation. Changes in signals that appear to be adaptations to avoid predation include the use of different signal modalities, changes in signaling behavior, loss of signals, and alteration of signal characteristics such as pitch. Selection pressure from signal exploiters could lead to the production of a novel signal and thus facilitate speciation. Relatively little work has been done on adaptations on the part of the exploiting species, but such adaptations could indirectly influence the mating system of the predator or parasitoid. Signal exploitation is also expected to be a fruitful source of examples of coevolution. Finally, plants emit attractants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation.
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Most plants combine sexual and clonal reproduction, and the balance between the two may vary widely between and within species. There are many anecdotal reports of plants that appear to have abandoned sex for clonal reproduction, yet few studies have quantified the degree of sexual variation in clonal plants and fewer still have determined the underlying ecological and/or genetic factors. Recent empirical work has shown that some clonal plants exhibit very wide variation in sexual reproduction that translates into striking variation in genotypic diversity and differentiation of natural populations. Reduced sexual reproduction may be particularly common at the geographical margins of species’ ranges. Although seed production and sexual recruitment may often be limited by biotic and abiotic aspects of the environment in marginal populations, genetic factors, including changes in ploidy and sterility mutations, may also play a significant role in causing reduced sexual fertility. Moreover, environmental suppression of sexual recruitment may facilitate the evolution of genetic sterility because natural selection no longer strongly maintains the many traits involved in sex. In addition to the accumulation of ‘neutral’ sterility mutations in highly clonal populations, the evolution of genetic infertility may be facilitated if sterility is associated with enhanced vegetative growth, clonal propagation or survival through either resource reallocation or pleiotropy. However, there are almost no experimental data with which to distinguish among these possibilities. Ultimately, wide variation in genotypic diversity and gene flow associated with the loss of sex may constrain local adaptation and the evolution of the geographical range limit in clonal plants.
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Asexual taxa are short-lived, suggesting that transitions to asexuality represent evolutionary dead-ends. However, with high rates of clonal origin and coexistence of asexuals and sexuals via selective asymmetries, asexuality may persist in the long term as a result of a dynamic equilibrium between clonal origin and extinction. Few such systems have been studied in detail. Here, we investigate the evolutionary history of asexual lineages of Daphnia pulex, which are derived from sexual relatives via the inheritance of a dominant female-limited meiosis-suppressing locus and inhabit ponds throughout northeastern North America (NA). Our extensive sampling and subsequent phylogenetic analysis using mitochondrial sequence data reveals a young and genetically diverse asexual assemblage, reflecting high rates of clonal origin due to the contagious nature of asexuality. Yet, asexuality is restricted to two phylogroups (B and C) with historical and/or present associations with northeastern NA and is absent from a northwestern phylogroup (A), supporting a recent northeastern origin of asexuality in this species. Furthermore, macrogeographic patterns of genetic variability indicate that phylogroups B and C recolonized northeastern NA from opposite directions, yet their presently overlapping geographic distributions are similarly divided into an eastern asexual and a western sexual region. We attribute these patterns to a recent contagious spread of asexuality from a northeastern source. If environment-mediated selective asymmetries play no significant role in determining the outcome of competitive interactions between sexuals and asexuals, regions of contact may be setting the stage for continued asexual conquests.