Download Sexual selection and genital evolution

bs_bs_banner
Austral Entomology (2014) 53, 1–17
Invited Review
Sexual selection and genital evolution
Leigh W Simmons*
Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, Crawley, WA
6009, Australia.
Abstract
Male genitalia show patterns of divergent evolution, and sexual selection is recognised as being responsible
for this taxonomically widespread phenomenon. Much of the empirical support for the sexual selection
hypothesis comes from studies of insects. Here, I synthesise the literature on insect genital evolution, and
use this synthesis to address the debate over the mechanisms of selection most likely to explain observed
patterns of macroevolutionary divergence in genital morphology. Studies of seven insect orders provide
evidence that non-intromittent genitalia are subject to sexual selection through their effects on mating
success, while intromittent genitalia are subject to selection through their effects on fertilisation success.
However, studies that use quantitative methods to analyse the form of selection are necessary to identify the
mechanisms of sexual selection involved. Phylogenetic analyses from diverse taxonomic groups confirm
that divergence in male genital morphology can be predicted from variation in the opportunity for sexual
selection. Much debate revolves around the importance of female choice and sexual conflict in the evolution
of male genitalia, the resolution of which lies in economic studies of mating interactions and in recognising
sexual selection as a continuum between male competition, sexual conflict and female choice. The species
isolating lock-and-key hypothesis is frequently dismissed as unimportant in genital evolution because in part
of a perceived lack of variation in female genitalia across species. Increasingly, however, studies report
species-specific variation in female genital morphology and its coevolutionary divergence with male genital
morphology. Contemporary views recognise a continuum between female choice that enforces species isolation and female choice that targets variation in male quality within populations, placing lock-and-key
processes into the realm of sexual selection. Distinguishing between species-isolating and directional forms
of female choice will require studies that examine both the tempo and mode of divergence, both within and
among species.
Key words
coevolution, female choice, genitalia, sexual conflict, sexual selection, species isolation.
I NTRODUCT IO N
Male genitalia are widely recognised as being the most variable and divergent of all morphological structures. Indeed,
male genitalia are considered one of the most important diagnostic traits in insect systematics (Tuxen 1970), and there are
entire groups whose classification is based solely on the
structure of male genitalia (Eyer 1924; Dirsh 1956). Hypotheses for why genitalia should exhibit such divergent evolution date back to Dufour (1848) who proposed that genital
morphology provides a prezygotic reproductive isolating
mechanism whereby species-specific male genitalia represent
a key to ‘unlock’ species-specific female genitalia. In contrast, Mayr (1963) argued that because genitalia are generally
internal structures, they should be protected from natural
selection and free to diverge at random because of
*[email protected]
© 2013 Australian Entomological Society
pleiotropic effects of selection acting on general morphology.
Waage’s (1979) pioneering work on damselfly genitalia
revealed the remarkable dual function of male genitalia,
whereby the male uses his intromittent secondary genitalia to
remove rival sperm from the sperm stores of recently mated
females before delivering his own ejaculate. This discovery
raised the intriguing possibility that sexual selection might be
a significant driving force behind the evolution of male genitalia (Lloyd 1979).
In his influential syntheses of the literature, Eberhard (1985,
1996, 2010) has championed the hypothesis that sexual selection is responsible for both rapid and divergent evolution of
male genital morphology. Moreover, he has argued that sexual
selection through Fisherian female choice offers the most
general explanation. Male genitalia are proposed to stimulate
females during copulatory courtship, and females choose
males cryptically by increasing offspring production or preferentially storing and using sperm from males better equipped
to provide the appropriate stimulation. Eberhard (1985)
doi:10.1111/aen.12053
2
L W Simmons
rejected the pleiotropy hypothesis on the firm grounds that in
many species, where males possess secondary structures
involved in copulation, such as the secondary intromittent
organs of dragonflies or the gonopods of millipedes, it is these
secondary copulatory structures that exhibit patterns of rapid
and divergent evolution, while the primary genitalia do not.
Eberhard (1985) also argued that Dufour’s lock-and-key
hypothesis cannot provide a general explanation for genital
evolution because female genitalia are generally simple in
their morphology, lacking any obvious structures that can act
as ‘locks’. Whether the lock-and-key hypothesis can ever be
rejected outright is debatable (Shapiro & Porter 1989). Indeed,
sexual selection via female choice can be an important
species-isolating mechanism (Ryan & Rand 1993; Higgie &
Blows 2007; Ritchie 2007) so that lock-and-key and sexual
selection arguments for genital evolution are not exclusive, a
point to which I shall return later in this review.
There are three principal mechanisms by which male
genital morphology might be under sexual selection
(Simmons 2001). As Eberhard (1985) first proposed, male
genitalia may be subject to selection via female choice. They
may also be involved in the avoidance of sperm competition
through their role in the physical removal or displacement of
rival sperm, and thus subject to sexual selection via malecontest competition. Furthermore, male and female interests
over fertilisation events often may differ. Female interests
may lie in the use of sperm acquired from males providing
greater copulatory stimulation, while male interests lie in
removing or displacing any rival sperm from the female’s
reproductive tract.
Divergent male and female interests can generate sexual
conflict as males and females struggle in an evolutionary arms
race to maximise their own fitness (Parker 1979; Arnqvist &
Rowe 2005). Distinguishing between these mechanisms of
sexual selection is not easy, and there has been considerable
debate over which sexual selection force might be more important in genital evolution (Eberhard 2004a, 2006, 2010). Nonetheless, regardless of the precise mechanisms involved, sexual
selection is now widely acknowledged as being a significant
force driving the evolution of animal genitalia (Hosken &
Stockley 2004), and much of the evidence for the sexual selection hypothesis comes from studies of insects. Here, I offer a
synthesis of the literature on the evolution of insect genitalia
and use this literature to address the debate over the mechanisms of selection that are most likely to explain observed
patterns of macroevolutionary divergence in insect genitalia
and animal genitalia more generally.
Empirical studies have adopted two approaches with
which to explore the role of sexual selection in genital evolution, within species studies of variation in male genital
morphology and its effect on individual reproductive success,
and comparative analyses of genital morphology across
species. Arnqvist (1997) advocated a within-species
approach that focused on exploring patterns of phenotypic
and genetic variation in genital morphology and their effects
on male fitness. Therefore, I start this review with an overview of my own research on a single species, the dung beetle
© 2013 Australian Entomological Society
Onthophagus taurus, which has proved a useful model
system for studying the evolution of genital morphology. A
broader review of the literature on single species studies
follows, which has provided evidence that sexual selection
can act on male genital morphology. Finally, I review evidence from comparative analyses that sexual selection acting
on male genitalia can account for the broad patterns of
macroevolutionary divergence we see in genital morphology.
I conclude by discussing current controversies over which
mechanisms most likely account for the evolutionary divergence of animal genitalia.
ON T H OPH AGIN E DUN G BEET L ES : A
MODEL S YS T EM F OR S T UDIES OF
GEN ITAL EVOL UT ION
Typical of insects generally, male genitalia have proven to be
remarkably useful morphological traits for dung beetle classification (Tarasov & Solodovnikov 2011). The aedeagus consists of two segments, the phallobase and the articulating
parameres (Fig. 1). The sample of aedeagi shown in Figure 1
illustrates that among species, there is considerable variation
in the relative lengths of the aedeagal segments and in the
shape of the parameres. Moreover, encased within the
phallobase are two groups of sclerites associated with the
endophallus, the lateral sclerites that form the lamella
copulatrix and the accessory sclerites. While homologous
sclerites can be found among onthophagines, the shape and
complexity of these sclerites are highly divergent (Fig. 2)
offering a strong phylogenetic signal for classification of the
group. Indeed, Tarasov and Solodovnikov (2011) found that
genital sclerites offered significantly fewer homoplasious (and
therefore phylogenetically informative) traits than did nongenitalic morphological traits. Onthophagine dung beetles
thus offer an excellent model system for exploring the evolutionary mechanisms of genital divergence.
Functional morphology of male genitalia
Any study of selection acting on morphological traits requires
an understanding of the functional morphology of those traits
(Fairbairn et al. 2003; Jagadeeshan & Singh 2006). During
courtship, the male Onthophagus taurus mounts the female
from behind and courts by drumming on her elytra and flanks
with his fore legs while probing the ventral surface of her
terminal segments with the extruded aedeagus. If receptive, the
female will open her genital tract by raising her pygidium,
allowing the male to anchor the distal hooks of the parameres
into pits located on its interior surface. Once genital contact is
established, the endophallus is everted into the female’s
genital tract (Werner & Simmons 2008). The endophallus is
held in situ by the fit of the paramere hooks into the female’s
genital pits, the inflated endophallus horn into the female’s
rectum and the grasping of the soft tissue of the bursa
copulatrix by the lamella copulatrix (Fig. 3). The axial,
subaxial and frontolateral sclerites form a functional unit that
Sexual selection and genital evolution
3
Fig. 1. Male aedeagus morphology of Onthophagus sp. The aedeagus of O. avocetta is shown with its associated endophalic sclerites
highlighted in different colours (from Tarasov & Solodovnikov 2011). Aedeagus outlines from Zunino (1979). AcS, accessory sclerites;
AMS, additional medial sclerite of lamella copulatrix; Blp, basolateral paramerite; Br, bristle; En, endophallus; IL, inferior left lobe of
lamella copulatrix; IR, inferior right lobe of lamella copulatrix; LC, Lamella copulatrix; PhFS, phallobase frontal side; PhRS, phallobase
rear side; PIS, paramere inferior side; PSS, paramere superior side; SL, superior left lobe of lamella copulatrix; SR, superior right lobe
of lamella copulatrix.
delivers the ejaculate to the bursa copulatrix. The sperm and
seminal fluid are contained within a tubular spermatophore,
which is moulded by the axial, subaxial and frontolateral
sclerites, with its opening positioned within the spermathecal
duct (Fig. 3). The superior right peripheral sclerite does not
appear to interact directly with the female being located inside
the endophallus. However, it may impart structural support for
the inflated endophallus and/or aid in maintaining the position
of the endophallus during copulation (Werner & Simmons
2008).
Selection on male genitalia
Quantitative methods for measuring the strength and form of
selection acting on morphological traits have been available
for some time (Arnold & Wade 1984a, b), yet with some
exceptions (Bertin & Fairbairn 2005), few studies of genital
evolution have used this method to explore patterns of selection. Estimates of the strength and form of selection acting on
the aedeagus of O. taurus via a male’s ability to engage the
female in copula have been conducted, following a landmarkbased geometric morphometric approach to capture variation
in aedeagus size and shape. Selection analyses revealed
significant directional sexual selection acting on the shape but
not the size of the aedeagus (Simmons et al. 2009; Simmons
& Garcia-Gonzalez 2011). Specifically, males with long, thin
parameres and a long phallobase are more successful in engaging the female in copula than males with short, stout aedeagus
segments (Fig. 4a). Aedeagus morphology was found to have
no significant impact on a male’s fertilisation success following copulation and thus appears to be subject to precopulatory
sexual selection only (Fig. 4b).
In contrast, variation in the morphology of the endophallus
sclerites was found to have a significant effect on competitive fertilisation success (House & Simmons 2003). Specifically, House and Simmons (2003) found that males with a
large frontolateral peripheral sclerite and a small lamella
copulatrix tended to have greater defensive paternity success
(first male to mate), while males with a large axial and small
superior right peripheral sclerite tended to have greater offensive (second male to mate) paternity success. These data can
tell us that individually, the genital sclerites can influence
paternity outcome when females mate multiply. However,
because of the morphological complexity of the genital
sclerites and their functional integration, these data cannot
© 2013 Australian Entomological Society
4
L W Simmons
Fig. 2. Male genital sclerite morphology of Onthophagus sp. The accessory sclerites of the endophalus are shown in detail for: (a,b)
O. taurus; (c,d) O. avocetta; (e,f) O. tricornis; and (g,h) O. mouhoti. Colours indicate homologous structures among species (from
Tarasov & Solodovnikov 2011). A, axial sclerite; FLP, frontolateral peripheral sclerite; InL, internal lobe; ExL external lobe; LP, lateral
process; MP, medial peripheral sclerite; SA, subaxial sclerites 1–3; SRP, superior right peripheral sclerite.
inform us of the strength or form of sexual selection acting
on the integrated functional unit. Fortunately, multivariate
approaches are available to assess selection acting on
complex suites of traits (Lande & Arnold 1983; Phillips &
Arnold 1989). Thus, Simmons et al. (2009) estimated multivariate selection acting on the endophallus sclerites in both
defensive and offensive contexts, revealing non-linear selection on four of five axes of variation from a canonical analysis of the matrix of non-linear selection gradients.
Visualisation of the fitness surface in Figure 5 clearly shows
that, collectively, the genital sclerites of the endophallus are
subject to strong stabilising selection. The strength of stabilising selection was found to be greatest in the defensive
context (Simmons et al. 2009).
© 2013 Australian Entomological Society
Evolutionary response to selection on
male genitalia
Unequivocal support for a role for sexual selection in the
evolutionary divergence of male genital morphology requires
evidence that the patterns of selection observed within
generations can generate changes in genital morphology
across generations. The technique of experimental evolution
offers a powerful approach for testing evolutionary hypotheses (Kawecki et al. 2012) and has been applied recently to
the hypothesis that sexual selection can drive the evolutionary divergence of male genital morphology using the
O. taurus model system (Simmons et al. 2009; Simmons &
Garcia-Gonzalez 2011).
Sexual selection and genital evolution
5
Fig. 3. Schematic representation of the
Onthophagus taurus endophallus fully
engaged with female genital structures:
(a) left view; (b) right view (from Werner
& Simmons 2008). 1, superior right
peripheral sclerite; 2/3, axial and subaxial
sclerites; 4, lamella copulatrix; 5,
frontolateral peripheral sclerite; bp,
bristle plate; en, endophallus; ov, oviduct;
pm, paramere of the aeadeagus; pyg,
pygidium; rec, rectum; sd, spermathecal
duct; sde, spermathecal duct extension;
sp, spermatheca.
a
Probability of mating
b
P2
Aedeagus shape (PC2)
Second male’s aedeagus shape (PC2)
Fig. 4. Selection acting on the Onthophagus taurus aedeagus. (a) cubic spline (with 95% confidence bands) visualisation of directional
selection gradient acting on aedeagus shape via a male’s ability to engage the female in copula (negative scores on the principal
component axis describes a long thin aedeagus) (from Simmons et al. 2009). (b) There is no significant relationship between the shape
of a male’s aedeagus and his offensive paternity success (P2) once copulation is achieved (standardised gradient = −0.03 ± 0.06,
F1,25 = 0.42, P = 0.525; LW Simmons unpublished data).
Simmons and colleagues established six experimental populations of beetles, randomly assigning three to breed
polygamously and three to breed monogamously. In polygamous populations, male and female beetles were allowed to
interact and mate freely before females produced their broods
(Simmons et al. 2009). Thus, there was the opportunity for
sexual selection to act on these populations, and indeed,
molecular screening of putative parents and the offspring
emerging from these populations confirmed that there was a
significant positive Bateman gradient – a measure of the
opportunity for sexual selection based on the relationship
between number of mates and relative male fitness (Simmons
et al. 2004; Simmons & García-González 2008). In monoga-
mous populations, a single male and female were allowed to
mate before the female produced her brood, so that there was
no opportunity for sexual selection to operate. All other
aspects of the populations’ life-histories were tightly
controlled.
Simmons and colleagues allowed their populations to
evolve under these monogamous and polygamous mating
regimes for 19 generations before quantifying variation in
male genital morphology, finding significant divergence in the
shape, but not size of the aedeagus (Fig. 6). The aedeagus
evolved to be longer and thinner in populations subject to
sexual selection, exactly the divergence we should expect
given the directional selection acting on aedeagus shape within
© 2013 Australian Entomological Society
L W Simmons
Aedeagus shape (PC2±SE)
6
Fig. 5. Stabilising selection acting on the endophallus sclerites
of the Onthophagus taurus aedeagus. Relative fitness is the fertilisation success of males mating in the defensive role of firts to
mate, standardised to the population average fertilisation success.
The axes m1 and m5 are the strongest positive and negative
eigenvectors from a canonical analysis of the matrix of standardised quadratic and correlational selection gradients. Axis m1
describes variation in the size and shape of the superior right
peripheral sclerite and the subaxial sclerites, while axis m5
describes variation in the size and shape of the axial and
frontolateral peripheral sclerites, and the lamella copulatrix (from
Simmons et al. 2009).
the source population (Fig. 4a). In contrast, no divergence was
found in the morphology of the endophallus sclerites
(Simmons et al. 2009). Again, this is to be expected from the
pattern of stabilising selection acting on the genital sclerites
(Fig. 5).
Experimental evolution thus provides unequivocal evidence
that sexual selection can generate a divergence in genital morphology among populations of the same species. But can
divergence occur among natural populations of beetles and
contribute to speciation? There is evidence to suggest that it
can. O. taurus originally was limited to a Turanic-EuropeanMediterranean distribution but was introduced into the eastern
states of North America and into Australia in the late 1960s
and early 1970s. Analyses of native and exotic populations of
O. taurus have revealed substantial divergence in aedeagus
shape among these allopatric populations (Pizzo et al. 2008).
Moreover, the same axes of shape variation distinguishes
native O. taurus populations from their sympatric closely
related sister species O. illyricus (Pizzo et al. 2008), and it is
interesting to note that more broadly, differences in aedeagus
morphology among Onthophagus sp. are characterised by
variation in the relative length and girth of the aedeagus segments (Fig. 1).
© 2013 Australian Entomological Society
Enforced
monogamy
Sexual
selection
Fig. 6. Evolutionary divergence in the shape of the
Onthophagus taurus aedeagus across three populations subjected
to enforced monogamy and three populations subjected to sexual
selection for 19 generations of experimental evolution. Positive
scores on PC2 characterise an aedeagus that is long and thin,
while negative scores characterise an aedeagus that is short and
stout (from Simmons et al. 2009).
Coevolution of female genitalia
Most hypotheses for the evolutionary divergence in male
genital morphology predict a coevolutionary divergence in
female genital morphology or the sensory traits that directly
recognise and respond to stimulation generated by male genitalia. Thus, the lock-and-key hypothesis would predict that
changes in female genital morphology should be closely
tracked by changes in male genital morphology. A classic
theoretical prediction underlying models of female choice is
that the female preference – the morphological, behavioural or
sensory mechanism by which females choose among males –
should coevolve with the preferred traits in males (Andersson
1994). Likewise, correlated evolution of male and female traits
is expected from the cycles of antagonistic coevolution that
characterise sexual conflict (Arnqvist & Rowe 2005). The
parameres of the O. taurus aedeagus and the genital pits on the
internal surface of the female’s pygidium are mechanically
coupled during copulation (Fig. 3), and this mechanical fit
might be expected to affect their mutual evolution. Simmons
and Garcia-Gonzalez (2011) quantified variation in the morphology of the female genital pits among their experimentally
evolving populations. They found that in populations subject
to sexual selection, the genital pits became smaller and their
Sexual selection and genital evolution
7
Fig. 7. Evolutionary divergence in the
configuration of the pygidial genital pits
of Onthophagus taurus among three
populations subjected to enforced
monogamy and three populations subjected to sexual selection for 19 generations of experimental evolution. The thin
plate splines come from a geometric
morphometric analysis of landmarks
placed around the edge of the pygidium
and the genital pits, and show how positive scores on the relative warp axis
describe pits that are reduced in size and
more moved away from the pygidium
edge (for more details, see Simmons &
Garcia-Gonzalez 2011).
position on the internal wall of the pygidium moved further
away from the pygidium edge, while the reverse was true for
populations subject to enforced monogamy (Fig. 7).
Thus, sexual selection appears to favour both the internalisation of the genital pits in females, which would make them
more difficult for males to reach, and the elongation of the
aedeagus in males that we know makes it easier for them to
reach the genital pits and engage the female in copulation
(Fig. 4a). Quantitative genetic analyses of male and female
genital configuration have also revealed significant genetic
correlations between male and female genital morphology, a
genetic architecture that is expected of traits undergoing concerted evolution (Simmons & Garcia-Gonzalez 2011). Finally,
studies of allopatric populations of O. taurus confirm that correlated divergence in male and female genital morphology
occurs among natural populations, and studies of
Onthophagus sp. in the O. fracticornis-similis-opacicollis
species complex have confirmed that concerted evolution of
male and female genital traits characterises speciation in this
complex (Macagno et al. 2011).
GE NITAL MO RPHO LO G Y G E NE RAL LY
AFFE CTS MALE FIT NE SS
There is now evidence from seven orders of insect that variation in male genital morphology can be a significant predictor
of male reproductive success and therefore be the focus of
sexual selection (Table 1). The earliest evidence that variation
among males in their genital morphology might predict male
reproductive success came from experimental studies of
tortoise beetles Chelymorpha alternans (Rodriguez 1995;
Rodriguez et al. 2004). The males of Chelymorpha sp. possess
an elongated genital flagellum that is threaded through the
length of the female’s spermathecal duct to the entry of the
spermatheca where sperm are stored. The male then deposits a
spermatophore in the bursa copulatrix and sperm migrate from
the spermatophore along the length of the genital flagellum to
the spermatheca. Rodriguez and colleagues shortened the flagellum of some males experimentally, finding that this
manipulation resulted in a reduction in the number of sperm
stored, an increase in the number of sperm dumped by the
female following copulation, and a decrease in the proportion
of offspring sired (Rodriguez 1995; Rodriguez et al. 2004).
Experimental manipulations of the size or length of genital
traits, either by their partial of complete ablation, is a frequently used method for assessing the impact of male genital
traits on mating and/or insemination success (Table 1). Such
approaches, however, tell us little about how selection acts on
genital morphology. By analogy, although removing the legs
of a long distance runner would show us that legs are required
to run, it would tell us little about how stride length contributes
to running speed. Nonetheless, such approaches can sometimes be useful in identifying the functional mechanisms by
which male genitalia might impact fitness. In Callosobruchus
maculatus, for example, the ablation of genital spines (or their
shortening via artificial selection) has the effect of reducing
the ability of males to perforate the female’s internal genital
tract walls, a process that is necessary for seminal fluid proteins to pass into the female’s circulatory system where they
act on her reproductive physiology in such a way as to increase
the copulating male’s paternity (Hotzy et al. 2012). In contrast, ablating genital spines has no impact on a male’s ability
to prolong copulation or his ability to transfer ejaculate to the
female (Hotzy et al. 2012). Arguably, the best evidence of the
potential for selection to act on variation in male genital morphology comes from studies that have examined how natural
variation in male genital size or shape affects male reproductive success.
A number of correlational studies have shown us that variation in male genital morphology can influence either male
mating success, the duration of copulation, the number of
sperm transferred to the female’s sperm storage organs or
paternity success (Table 1). In the Australian mantid genus
© 2013 Australian Entomological Society
© 2013 Australian Entomological Society
Mating success
Mating success
Paternity
Copula duration & mating speed
Paternity
Sperm transfer
Sperm transfer and paternity
Mating success
Paternity
Aedeagal spicule
Genital sclerite length
Genital spines
Copulatory piece length
Genital flagellum length
Aedeagus shape
Genital sclerites
Genital clasper asymmetry
Aedeagus length
Mating success
Copula duration
Paternity
Paternity
Sperm transfer
Mating success
Genital length
Genital width
Genital sclerites
Genital sclerites
Processus gonopori length
Genital claspers
Paternity
Mating success
Mating success
Mating success
Sperm storage, female remating
Sperm storage, ovulation, female remating
Copula duration & paternity
Length of virgae
Genital clasper length & asymmetry
Genital spine length
Genital spine length
Clasper
Median cercal hooks
Lateral cercal teeth
Sperm transfer
Dorsal left complex & right phalomere
Correlational
Correlational
Correlational
Ablation
Ablation
Correlational
Ablation
Ablation
Correlational
Correlational
Ablation & selection
Ablation
Ablation
Correlational
Correlational
Correlational
Correlational
Correlational
Correlational
Correlational
Ablation
Correlational
Correlational
Ablation
Correlational
Correlational
Evidence
Koshio et al. (2007)
Xu and Wang (2010)
Otronen (1998)
Grieshop and Polak (2012)
Kamimura and Polak (2011); Polak and Rashed (2010)
Blanckenhorn et al. (2004)
Briceño and Eberhard (2009b)
Briceño and Eberhard (2009a)
Wenninger and Averill (2006)
Sakurai et al. (2012)
Hotzy et al. (2012)
Takami (2003)
Rodriguez (1995); Rodriguez et al. (2004)
Simmons et al. (2009)
House and Simmons (2003); Simmons et al. (2009)
Bertin and Fairbairn (2005)
Gagnon and Turgeon (2011)
Danielsson and Askenmo (1999)
Arnqvist and Danielsson (1999)
Tadler (1999); Tadler and Nemeschkal (1999)
Moreno-Garcia and Cordero (2008)
van Lieshout (2011); van Lieshout and Elgar (2011)
Holwell et al. (2010)
Tsuchiya and Hayashi (2008)
Córdoba-Aguilar (1999, 2002)
Córdoba-Aguilar (2009)
Source
Studies are categorised as ‘ablation’ if they involved the surgical reduction or removal of male genital features, or ‘correlational’ if they examined the effect of natural variation in measures of male genital traits.
Diptera
Dryomyza anilis
Drosophila ananassae
Drosophila bipectinata
Sepsis cynipsea
Glossina marsitans
Glossina pallidipes
Lepidoptera
Elcysma westwoodii
Ephestia kuehniella
Sperm displacement
Sperm displacement
Sperm displacement
Affect
Spiny lateral horns of adeagus
Aedeagus width
Aedeagus width
Trait
Studies on the fitness consequences of variation in male genital morphology for male mating and fertilisation success
Odonata
Calopteryx cornelia
Calopteryx haemorrhoidalis
Hetaerina americana
Mantodea
Ciulfina klassi
Dermaptera
Euborellia brunneri
Hemiptera
Aquarius remigis
Gerris gillettei
Gerris lacustris
Gerris lateralis
Lygaeus simulans
Stenomacra marginella
Coleoptera
Anomala orientalis
Callosobruchus chinensis
Callosobruchus maculatus
Carabus insulicola
Chelymorpha alternans
Onthophagus taurus
Species
Table 1
8
L W Simmons
Sexual selection and genital evolution
Ciulfina, for example, the ventral left complex and the right
phallomere of the male’s genitalia are involved both in physically opening the genital tract of the female and in the insertion
of the spermatophore (Holwell & Herberstein 2010). In
Ciulfina klassi, quantitative variation in the shapes of these
structures are correlated with the number of sperm transferred
by the male (Holwell et al. 2010). The studies in Table 1 also
show us that, as seen in dung beetles, different genital structures can influence different stages of reproduction. Thus, in
Gerris water striders, the genitalia consist of both nonintromittent and intromittent structures. The length of the nonintromittent structure is under sexual selection in both natural
and experimental populations, in which males with a longer
pygophore and proctiger have a greater mating success
(Preziosi & Fairbairn 2000; Fairbairn et al. 2003; Bertin &
Fairbairn 2005, 2007). The intromittent phalotheca has three
genital sclerites – the ventral, lateral and dorsal sclerites – the
shape of which influence a male’s competitive paternity
success when females have mated with more than one male
(Arnqvist & Danielsson 1999; Danielsson & Askenmo 1999).
Some studies identified in Table 1 can inform us of the
functional morphology of male genitalia. For example for the
damselfly Calopteryx haemorrhoidalis, Córdoba-Aguilar
(1999, 2002) showed how aedeagus width influenced the
number of rival sperm that were ejected from the female’s
sperm storage organs and ultimately removed from her reproductive tract at the end of copulation. The male’s aedeagus
stimulates the female’s sensory system that controls egg fertilisation and laying. Stimulation of the reproductive tracts of
target species basal in the phylogeny to Calopteryx
haemorrhoidalis with the Calopteryx haemorrhoidalis
aedeagus likewise induced sperm ejection, even though
conspecific aedeagi were unable to do so. This example
strongly suggests that the Calopteryx haemorrhoidalis
aedeagus has evolved to exploit the sensory system of females
(Córdoba-Aguilar 2002) and that the selective mechanism
involves the engagement in sperm competition by males
(removal of rival sperm), the action of female choice (sensory
perception and expulsion of sperm by females) and the potential for sexual conflict (Córdoba-Aguilar 2005). Nonetheless, it
is not clear if selection on aedeagus width in Calopteryx
haemorrhoidalis is directional for increasing aedeagus width
or stabilising for some optimal species-specific width.
Thus, while there is now good evidence that male genital
morphology can influence male reproductive fitness, it is also
clear that different genital traits can be subject to different
episodes of sexual selection, either precopulatory or
postcopulatory. Importantly, few studies in Table 1 have characterised the form of sexual selection acting on genital morphology. This is unfortunate because without an understanding
of the form of selection, we are unable to distinguish between
putative mechanisms underlying genital evolution. If we are to
move forward, future studies will need to adopt the quantitative framework of Lande and Arnold (1983) and Arnold and
Wade (1984b) for characterising the relative strengths of linear
and non-linear sexual selection acting on male and female
genitalia.
9
COMPARAT IV E AN ALYS ES OF GEN ITAL
EVOL UT ION AMON G S PECIES
Divergence in male genital morphology
If sexual selection is generally responsible for the evolution
of male genital morphology, we should expect to see
macroevolutionary patterns of divergence in genital shape and
size that depend on the opportunity for and strength of sexual
selection. Thus, in monogamous species, where females mate
with only a single male, the opportunity for sexual selection to
act on genital morphology during and after copulation is
limited, so we should expect monandrous taxa to exhibit far
less evolutionary divergence in genital morphology than polyandrous taxa. This expectation seems to be upheld by studies
of Heliconius butterflies (Eberhard 1985), apoid bees
(Roig-Alsina 1993) and ischnuran damselflies (Robinson &
Novak 1997; Simmons 2001). Of course, monandrous species
can diverge in genital morphology, as for example in the bumblebee genus Bombus (Richards 1927b). Male contest competition for females can be particularly intense in monandrous
species, where males struggle to gain and maintain genital
contact with females at emergence or feeding sites, or in
mating swarms (Thornhill & Alcock 1983). Sexual selection is
likely to act strongly on male genital traits that facilitate coupling and/or decrease the probability of take-overs by rival
males prior to insemination, and sexual selection can favour
the evolution of complex genital traits that allow males to
monopolise access to monandrous females (Richards 1927a;
Thornhill & Alcock 1983; Simmons 2001). Nonetheless, we
see in Table 1 that some genital traits are subject to sexual
selection via mating success, while others are subject to
postcopulatory sexual selection. Thus, we should expect
intromittent genitalia to show particularly strong patterns of
divergence because of mating system differences because it is
only in polyandrous taxa that postcopulatory sexual selection
also will operate. Indeed, among species in the grasshopper
genus Melanoplus, non-intromittent genitalia exhibit significantly less divergence than do intromittent genitalia (Márquez
& Knowles 2007).
Arnqvist (1998) provided strong evidence for the role
of sexual selection acting on genital divergence in his
phylogenetically controlled comparative analysis of insects
from four orders: Ephemeroptera, Diptera, Lepidoptera and
Coleoptera. Arnqvist (1998) calculated a morphometric distance, as the mean distance in multivariate trait space for a
species from the generic mean genital configuration. He then
calculated a distance ratio, as the mean distance for polyandrous genera divided by the mean distance for monandrous
genera for 19 phylogenetically independent clades. On
average, polyandrous clades were twice as divergent in
genital morphology than monandrous clades, as might be
expected given the greater opportunity for sexual selection in
polyandrous species. In contrast, non-genital morphological
traits did not differ in their degree of divergence among
monandrous and polyandrous clades. This study provides
strong evidence that sexual selection is responsible for the
© 2013 Australian Entomological Society
10
L W Simmons
evolutionary divergence in male genitalia generally. Patterns
of genital divergence among closely related species have
also been linked to more fine-grained variation in mating
system.
In their comparative analysis of ground beetles belonging
to the subgenus Ohomopterus (genus Carabus), Takami and
Soto (2007) documented significant positive correlated evolution between the length of the male copulatory piece and
spermatophore size, and significant negative correlated evolution between copulatory piece length and copulation duration. Within species the length of the copulatory piece
determines the speed of copulation, the correct placement of
the spermatophore within the female reproductive tract and
ultimately insemination success (Takami 2003). Likewise,
male genital titillators exhibit correlated evolution with copulation duration across species of bushcrickets (Tettigoniidae)
(Vahed et al. 2011). Species with male genital titillators have
longer periods of genital coupling prior to spermatophore
transfer than species without titillators, and titillator complexity influences the relationship between copulation duration and spermatophore size. Such patterns are difficult to
interpret without knowledge of the functional morphology of
genital traits, but they do show us that the evolutionary divergence in male genital morphology can be tightly linked with
the evolution of mating behaviour. Comparative studies
across species of water striders, where we have a detailed
understanding of the functional morphology of genital traits
and selection acting on those traits, have offered far greater
insight.
Rowe and Arnqvist (2012) conducted a comparative analysis of the shape and complexity of both non-intromittent and
intromittent male genitalia across 15 water strider species from
the genus Gerris. Their analysis yielded four important findings. First, genital shape and complexity exhibited a greater
evolutionary divergence than general morphological traits, and
intromittent genital traits exhibited greater divergence than
non-intromittent traits. Second, measures of complexity generally exhibited a strong phylogenetic signal, while measures
of shape did not, suggesting that shape may be evolving more
rapidly than complexity. Third, the divergence in intromittent
and non-intromittent genital traits was uncorrelated, suggesting that these different genital traits are subject to different
selection pressures. Indeed, Rowe and Arnqvist’s analysis
strongly supported findings from the single-species studies
of waterstriders highlighted in Table 1, that intromittent genitalia are subject to postcopulatory sexual selection, while
non-intromittent genitalia are subject to precopulatory sexual
selection.
Both groups of genital traits exhibited correlated evolution
with female mating rate, indicating that stronger sexual selection generated greater divergence in intromittent and nonintromittent genitalia. However, there was positive correlated
evolution between non-intromittent genitalia and sexual size
dimorphism, a proxy for the intensity of precopulatory sexual
selection (Arnqvist & Rowe 2002) but no correlated evolution
between non-intromittent genitalia and the sizes of male reproductive accessory glands and testes, a widely used proxy for
© 2013 Australian Entomological Society
the level of postcopulatory sexual selection (Simmons &
Fitzpatrick 2012). This pattern makes sense, given what we
know about selection acting on non-intromittent genitalia
during premating struggles in this genus (Preziosi & Fairbairn
2000; Fairbairn et al. 2003; Bertin & Fairbairn 2005, 2007).
The reverse pattern was true for intromittent genital traits;
there was no correlated evolution between the shape of
intromittent genital traits and sexual size dimorphism, but significant positive correlated evolution between the shape of
intromittent genitalia and male reproductive accessory gland
size. Again, this pattern is consistent with what we know about
the influence of genital sclerites on male fertilisation success
in this genus (Arnqvist & Danielsson 1999; Danielsson &
Askenmo 1999). These macroevolutionary patterns among
water striders, together with the differences in selection pressures on intromittent and non-intromittent genital traits found
in single-species studies of dung beetles and water striders,
support the general expectation that different genital traits can
be subject to very different sexual selection pressures
(Simmons et al. 2009).
Coevolutionary divergence in female
genital morphology
Eberhard (1985, 2010) has argued that the lock-and-key
mechanism cannot provide a general explanation for the divergent evolution of male genitalia because females do not
possess species-specific genitalia that could constitute the
required ‘lock’. However, this claim may be more apparent
than real. There is an extraordinary amount of data on male
genital morphology that has been derived from the taxonomic
literature (Eberhard 1985, 2004a,b). In contrast, female genital
structures have been inadequately studied by taxonomists
perhaps because they are frequently internal and require
destructive sampling. Not surprisingly, studies that have relied
largely on the taxonomic literature have failed to find evidence
for widespread coevolutionary divergence of male and female
genitalia (Eberhard 2004b, 2006). However, there is now a
growing body of evidence to suggest that females do possess
species-specific genital traits and that female genitalia can
exhibit patterns of divergent evolution that match those seen in
male genitalia.
In the scarab beetle Phyllophoga hirticula, female genitalia
are more complex than male genitalia (Polihronakis 2006) and
show greater divergence among populations (Polihronakis
2009). Among sepsid flies the internal female genitalia appear
to be evolving faster than either molecular or behavioural
characters (Puniamoorthy et al. 2010), and both male and
female genital traits contribute significant phylogenetic signals
for the classification of the hemipteran family Lophopidae
(Soulier-Perkins 2001). In Lepidoptera, signa (sclerotised
teeth within the female reproductive tract) are associated with
polyandrous mating systems, and the evolution of monandry is
associated with an evolutionary loss of the signa (Sánchez
et al. 2011). Importantly, there is growing evidence for the
widespread coevolutionary divergence of male and female
genital morphology (Table 2).
Sexual selection and genital evolution
11
Table 2 Studies of coevolution between male and female genital morphology
Taxon
Odonata
Calopteryx spp.
Enallagma spp.
Hemiptera
Gerris gillettei
Gerris incognitus
Gerris spp.
Coridromius spp.
Coleoptera
Callosobruchus spp.
Male trait
Female trait
Method
Source
Aedeagus width
Terminal abdominal cerci
Sensillum number
Mesostigmal plates
Species comparison
Phylogenetic analysis
Córdoba-Aguilar (2005)
McPeek et al. (2009)
Non-intromittent genital length
Non-intromittent genital size
and shape
Non-intromittent genital shape
Intromittent genital complexity
Connexival spines
Connexival spine size
and shape
Connexival spine shape
Paragenitalia complexity
Population comparison
Population comparison
Gagnon and Turgeon (2011)
Perry and Rowe (2012)
Phylogenetic analysis
Phylogenetic analysis
Arnqvist and Rowe (2002)
Tatarnic and Cassis (2010)
Genital spines
Phylogenetic analysis
Rönn et al. (2007)
Experimental evolution
Onthophagus taurus
Aedeagus shape
Copulatory duct
connective tissue
Genital pits
Onthophagus taurus
Onthophagus spp.
Diptera
Drosophila spp.
Drosophila spp.
Aedeagus shape
Aedeagus shape
Genital pits
Genital pits
Population comparison
Species comparison
Simmons and
Garcia-Gonzalez (2011)
Macagno et al. (2011)
Macagno et al. (2011)
Basal processes
Epandrial posterior lobe
Phallic spike
Phallic hook
Phallic spines
Cercal teeth
Aedeagal filament length
Genital cavities
Oviscapt pouch
Oviscapt furrow
Vulval shield
Uterine shield
Ventral vaginal shield
Spermathecal duct length
Species comparison
Phylogenetic analysis
Kamimura (2012)
Yassin and Orgogozo (2013)
Species comparison
Ilango and Lane (2000)
Phlebotomine flies
Comparative studies are categorised based on whether they involved appropriate phylogenetic control for common ancestry among species
(phylogenetic analysis) or not (species comparisons). Within species, studies are categorised based on whether they involved population comparisons or
laboratory experimental evolution.
Single species studies of the dung beetle O. taurus
revealed how internal female genital structures that interact
with the male’s aedeagus can diverge in response to experimental manipulation of sexual selection pressures (Fig. 7)
(Simmons & Garcia-Gonzalez 2011). A recent detailed
examination of the female reproductive tracts of nine species
in the Drosophila melanogaster subgroup discovered five
female genital traits that are species-specific in form and that
exhibit significant coevolution with distinct male genital features (Yassin & Orgogozo 2013). Likewise, in Gerris water
striders, female abdominal spines exhibit significant
coevolutionary divergence with male non-intromittent genitalia involved in grasping females during copulatory attempts
(Arnqvist & Rowe 2002). Patterns of coevolutionary divergence are seen both among species and among populations
within species (Table 2), and they are not limited to insects
(Brennan et al. 2007; Kuntner et al. 2009; Evans et al. 2011;
Burns et al. 2013). The coevolution of male and female genitalia can be facilitated if they share a common genetic architecture, as seems to be the case for dung beetles (Simmons &
Garcia-Gonzalez 2011) and ground beetles (Sasabe et al.
2010). Clearly, female genital morphology is an important
yet neglected aspect of studies that aim to determine the
causes of divergent evolution in male genital morphology.
Greater efforts need to be made in characterising female
genital structures, exploring how female genitalia interact
with male genitalia during copulation, and in determining
patterns of phenotypic and genotypic variation in female
genitalia and their covariation with male genitalia.
DIS T IN GUIS H IN G BET W EEN
MECH AN IS MS OF S EL ECT ION
Early studies of genital evolution used patterns of allometric
scaling to infer the form of selection acting on male genital
morphology. Directional sexual selection is thought to generate positive allometric scaling of traits under selection, a
pattern often associated with male secondary sexual traits
(Petrie 1988; Wilkinson 1993; Simmons & Tomkins 1996;
Wilkinson & Taper 1999). In contrast, stabilising selection
favours intermediate values of a trait irrespective of body size,
which will reduce trait size variation and generate negative
allometry (Eberhard et al. 1998). Indeed, strong stabilising
selection is expected to generate patterns of canalised growth,
in which traits are protected from environmental perturbations
that affect adult body size (House & Simmons 2007).
In addition to their divergent evolution, a second striking
pattern is that insect genitalia generally exhibit negative
allometric scaling (Eberhard et al. 1998; Hosken et al. 2005;
Eberhard 2009), suggesting that genital size is subject to widespread stabilising selection: Eberhard et al.’s (1998) ‘one-sizefits-all’ hypothesis. Single species studies have found that male
genitalia exhibit canalised patterns of growth (Dreyer &
Shingleton 2011). In the dung beetle O. taurus for example,
sexually selected head horns showed plasticity in size and
allometry in response to variation in nutritional environment,
but genital traits were highly invariant (House & Simmons
2007). In the hemipteran treehopper Enchenopa binotata,
genotype-by-environment interactions were found to be
© 2013 Australian Entomological Society
12
L W Simmons
strongest in sexual signals and weakest in genital traits, which
were again highly canalised (Rodríguez & Al-Wathiqui 2011,
2012). Theoretically, these general patterns could arise from
widespread stabilising selection acting on male genitalia.
However, inferring mechanisms of selection from patterns of
allometric variation is problematic (Bonduriansky & Day
2003; Bonduriansky 2007).
Studies of water striders, Aquarius remigis, show that nonintromittent genitalia exhibit negative allometry and low levels
of variation despite strong and persistent directional sexual
selection (Bertin & Fairbairn 2007). Experimental evolution
studies offer conflicting results. Experimental manipulation of
sexual selection in dung beetles, O. taurus, did not generate
divergence in the size of either non-intromittent or intromittent
genital traits, or in their allometric scaling (Simmons et al.
2009). A similar study of seed beetles, Callosobruchus
maculatus, did find an evolutionary reduction in the allometric
scaling of genital spines in populations from which sexual
selection had been experimentally removed via enforced
monogamy (Cayetano et al. 2011). While this result suggests
that sexual selection maintained elevated allometric scaling,
the form of selection acting on genital spines remains unclear.
Collectively, these studies show that patterns of allometric
scaling alone can be unreliable for inferring the mechanisms of
selection acting on genital traits.
Much effort has been spent in attempting to distinguish
between mechanisms of sexual selection. Eberhard’s (1985)
original hypothesis was based on traditional Fisherian female
choice, whereby females favour males with certain genitalic
forms because they are more ‘attractive’ during copulatory
courtship, and by favouring such males, females will produce
more attractive sons and daughters with the preference for
genital stimulation. The hypothesis has its foundation on indirect benefits of female choice. Sexual conflict (Parker 1979)
has become widely recognised as an important mechanism of
sexual selection acting on male genitalia (Arnqvist & Rowe
2005). Male traits, evolved in the context of sperm competition
or female genital stimulation, often can be damaging to
females. For example, the intromittent genitalia of sepsid flies
and seed beetles can rupture the internal reproductive tract of
the female, leading to a reduction in female lifespan
(Crudgington & Siva-Jothy 2000; Blanckenhorn et al. 2002).
Such mating costs can favour counter adaptations in females,
such as the thickening of the female reproductive tract wall to
prevent genital damage in seed beetles (Rönn et al. 2007).
Under the right conditions, male and female
counteradaptations can generate sustained cycles of sexually
antagonistic coevolution between male and female genital
morphology (Parker 1979).
The empirical evidence presented in this review of insect
genital evolution is consistent with most models of sexual
selection; female choice, sperm competition and sexual conflict models all predict that variation in genital morphology
should influence paternity, that multiple mating by females –
and thus the opportunity for these mechanisms of sexual selection to act – should be positively correlated with the degree of
genital divergence, and that there should be a correlated evo© 2013 Australian Entomological Society
lution of male and female genital morphology. None of these
mechanisms of sexual selection are mutually exclusive
(Simmons 2001); for example, female choice represents a key
component of sexual conflict (Arnqvist & Rowe 2005). Nonetheless, Eberhard suggests that the current evidence for sexual
conflict being generally important for genital evolution is relatively weak.
He based this argument on three qualitative surveys of insect
genital morphology. First, when classifying insect species as
either protected (species where females control mating activity) or unprotected (species where males control mating), he
found that there was no difference in the proportion of species
with species-specific male genitalia (Eberhard 2004a). This is
not a strong test because female choice in ‘protected’ species
could favour genital divergence of equal magnitude to sexual
conflict in ‘unprotected’ species. Second, he found little evidence of an evolutionary divergence of female traits that might
interact with male traits (Eberhard 2004b). However, as noted
earlier, detailed studies of the functional morphology of
female genital traits are rare. Those that have recently
appeared are revealing considerable variation in female genital
traits and their coevolution with male genital traits.
Even among species of insects in which sexual conflict is
likely to be strong, Eberhard (2006) found male genital morphology was only weakly divergent and genital traits tended to
be less complex than found among insects generally. Largescale surveys such as these are certainly useful in revealing
pattern, but they can provide very little evidence of process. A
key distinction between classic female choice and sexual conflict mechanisms lies in the costs and benefits to females from
their interactions with males, and as such economic studies are
required to distinguish between them (Fricke et al. 2009).
The importance of economic studies can be illustrated
with two examples. Single species studies of the dung beetle
O. taurus have shown us how male and female genital traits
exhibit a coevolutionary divergence under sexual selection
that could be due to sexual conflict or female choice alone
(Simmons & Garcia-Gonzalez 2011). Under sexual conflict,
genital pits are expected to evolve in such a way as to minimise male mating ability because of the costs of multiple
mating for females, while the males’ aedeagus evolves to
more effectively engage females in costly copulation. In contrast, a process of female choice alone predicts that by
choosing among males, females mate only with the best
males that can convey their mating ability (sexy sons) and
other potential genetic qualities to their offspring, providing
females with a net fitness gain.
Two lines of evidence suggest that for these beetles,
female choice is the most likely mechanism of sexual selection. First, among experimentally evolving populations,
sexual selection improved offspring condition (Simmons &
García-González 2008). Second, and most importantly,
females exposed to attractive males mated more frequently,
and both mating frequency per se and mating with attractive
males in particular increased the viability of offspring produced at no apparent cost to female fecundity or longevity
(Simmons & Holley 2011). These data show that repeated
Sexual selection and genital evolution
mating interactions are beneficial for females and that sexual
selection acting on male and female genitalia is most likely
to reflect female choice.
In contrast, work on water striders shows that mating is
costly for females (Rowe 1994; Arnqvist & Rowe 1995) and
that the coevolution of male grasping genitalia and female
antigrasping spines is most likely the consequence of antagonistic coevolution (Rowe & Arnqvist 2012). As noted repeatedly, it is highly unlikely that different mechanisms of sexual
selection will operate in isolation. Rather, dung beetles and
water striders are likely to represent cases that lie at either
extreme of a pure female choice-sexual conflict spectrum,
making attempts to identify one general mechanism of sexual
selection acting on insect genitalia biologically unrealistic.
Arguably, the same is true of debates over the importance,
or lack thereof, for species isolating lock-and-key mechanisms
in genital evolution. Eberhard (1985, 2010) dismisses lockand-key on the grounds that tight morphological fits between
male and female structures are not a general feature of insect
genitalia. Nonetheless, Eberhard et al.’s (1998) one-size-fitsall hypothesis arguably is congruent with a species isolation
mechanism in which stabilising selection favours a speciesspecific male genital size to fit the species-specific size of the
female genital tract. Moreover, tight morphological fits need
not characterise a female’s lock, which could be sensory in
nature (Patterson & Thaeler 1982; Eberhard 1985) or could
involve only those parts of the female reproductive tract that
actually contact male genital traits. Cryptic traits within the
internal genital tract of females are being found increasingly,
and these traits are highly divergent and coevolving with male
genital traits (e.g. Yassin & Orgogozo 2013).
Eberhard (2010) also cites a lack of character displacement
among males in zones of sympatry of closely related species as
evidence against a general role of species isolation mechanisms in genital evolution. Nonetheless, evidence of this type
is mixed. In stag beetles (Kawano 2003) and rhinoceros
beetles (Kawano 2002), there is greater genital character displacement in sympatry than allopatry. Among Carabus ground
beetles, variation in the size of the copulatory piece imposes
mechanical isolation between species (Sota & Kubota 1998).
However, Nagata et al. (2009) suggest that character displacement is unlikely in these species as there is little indication of
secondary contact between divergent forms of Carabus
arrowianus or evidence for greater divergence between populations close to the species boundaries.
Similarly, in Ciulfina mantids, geographic variation in male
genital morphology is unrelated to the location of populations
relative to species contact zones (Holwell 2008). In contrast,
Bath et al. (2012) found evidence that genital morphology
imposed asymmetric reproductive isolation between the Australian neriid flies Telostylinus lineolatus and Telostylinus
angusticollis, while Richmond et al. (2012) report less
genital variation within species than among species of the
diverging Drosophila mojavensis species cluster. Clearly,
some species or species groups show evidence of genitalia
being involved in reproductive isolation while others may
not. As Eberhard (2010) concedes, the possibility that a
13
lock-and-key mechanism applies in some cases cannot be discarded without careful study.
Contemporary views recognise a continuum between
female choice that enforces species isolation and female
choice that targets variation in male quality within populations
(Endler 1989; Ryan & Rand 1993; Endler & Houde 1995;
Castellano & Cermelli 2006; Higgie & Blows 2007). That is,
rather than being an alternative to sexual selection, a species
isolating lock-and-key mechanism should be viewed as one
end of the continuum of female choice. The question is how to
identify these modes of female choice and their relative
strengths. Patterns of stabilising selection acting on genitalia
and coevolutionary divergence between male and female
genital traits are both expected from a mechanism of selection
driven by species isolation. Stabilising female choice is
expected to result in very slow evolutionary divergence
between speciation events and a punctuated pattern of evolutionary change. In contrast, directional female choice should
generate rapid and continuous patterns of divergence among
species (McPeek et al. 2008).
We often see claims in the literature that male genital morphology is undergoing both rapid and divergent evolution, but
what evidence is there that genital evolution has been rapid?
The answer is very little. Few studies have actually quantified
both the tempo and mode of genital evolution. In their study of
Enallagma damselflies, McPeek et al. (2008) contrasted the
divergence in secondary male genital structures – the terminal
cerci used to grasp the female during copula – to models of
Brownian motion and punctuated equilibrium, finding that the
cerci were diverging following a model of punctuated equilibrium. Correlated divergence in female traits grasped by males
– mesostigmal plates – showed similar patterns of punctuated
evolution (McPeek et al. 2009), supporting a role of speciesisolating female choice in this group of damselflies. In contrast, a similar approach using Timema stick insects supported
a model of continuous evolutionary divergence and directional
sexual selection (Arbuthnott et al. 2010). Approaches such as
these offer great potential for distinguishing between putative
mechanisms of sexual selection. But what options are there for
estimating the rates of divergence in single species studies?
Techniques are available for estimating the rates of evolutionary divergence in morphological traits among isolated
populations of single species, but these have not yet been
widely adopted in studies of genital evolution. Contrasts
between genetic divergence at neutral loci – FST – and divergence in quantitative traits – QST – can provide an indication of
the rates of divergence in morphological traits (Brommer
2011; but see Merilä & Crnokrak 2001; McKay & Latta 2002;
Whitlock 2008; Edelaar et al. 2011; Lamy et al. 2012). When
FST equals QST, random genetic drift is sufficient to explain
morphological divergence. When QST exceeds FST, morphological traits can be inferred to be diverging more rapidly than
would be expected from neutral divergence and thus subject to
directional selection, and when FST exceeds QST, morphological traits are diverging more slowly than would be expected
from neutral genetic divergence and as would be expected
from strong stabilising selection.
© 2013 Australian Entomological Society
14
L W Simmons
Only one study of genital evolution has adopted this
approach so far, and that was a study of Australian millipedes
Antichiropus variabilis (Wojcieszek & Simmons 2012). In
these millipedes, the males secondary genitalia – the gonopods
– afford a tight fit with the genital tract of the female
(Wojcieszek et al. 2012), and they are under stabilising selection within populations (Wojcieszek & Simmons 2012).
Among isolated populations of these millipedes, male genitalia have diverged more slowly than would be expected from
neutral divergence (Wojcieszek & Simmons 2012). These patterns suggest strongly that the male genitalia are under
species-isolating female choice. Indeed, in experimental
crosses between populations, male genitalia contribute to a
mechanical reproductive isolation (Wojcieszek & Simmons
2013).
Traits that evolve rapidly are expected to provide a lower
phylogenetic signal than traits that evolve slowly (Losos
1999). Thus, across 41 cladistic analyses of insects, Song and
Bucheli (2010) found that genital traits were just as
phylogenetically informative as non-genital traits, suggesting
that genital traits might not be subject to a particularly rapid
divergence. Does this mean that species-isolating female
choice is of greater general importance in insect genital evolution? The answer is probably no. Rowe and Arnqvist (2012)
show that the strength of phylogenetic signal may depend on
how genital traits are characterised. Thus, among Gerris water
striders, they found that genital complexity – measured as the
presence/absence of substructures typical of cladistic analyses
– showed a strong phylogenetic signal, while quantitative variation in the shape of genital structures did not (Rowe &
Arnqvist 2012). This suggests that different genital features
may be subject to different rates of evolutionary divergence
and are perhaps subject to different forms of female choice.
CONCLUDIN G RE MARKS
Considerable evidence now exists that sexual selection is
responsible for a general and widespread divergence in male
genital morphology. Nonetheless, as a recent experimental
evolution study of Drosophila simulans illustrates, it is important to recognise that natural selection will also contribute to
the evolution of genitalia and sometimes oppose sexual selection (House et al. 2013). Research attention now focuses more
on distinguishing between the mechanisms of sexual selection
involved rather than whether sexual selection is important.
Sexual selection should be viewed as a continuum between
male contest competition, sexual conflict and pure female
choice, and it is unrealistic to expect that one particular
mechanism of sexual selection will prove to be generally more
important than another.
Moreover, it is time to recognise that female choice often
acts as a species-isolating lock-and-key mechanism in addition
to imposing directional selection on male genitalia within
populations. Different genital traits – intromittent or nonintromittent, size, shape, complexity – can be subject to different tempos and modes of selection even within the same
© 2013 Australian Entomological Society
species. Few studies examine the rates of genital evolution
despite the general claim that genitalia evolve rapidly. Progress in our understanding of genital evolution will be
achieved from a greater focus on the functional morphology of
female genitalia, an increased use of quantitative methods of
assessing the strength and form of selection acting on both
male and female genitalia, and an increased use of modern
comparative methods for exploring tempos and modes of evolutionary divergence. What is clear is that the patterns of
sexual selection acting on genital morphology are every bit as
complex as the traits they produce.
ACK N OW L EDGEMEN T S
I thank David Hosken, Nic Tatarnic and Jon Evans for comments on earlier drafts and the Australian Research Council for
financial support.
REF EREN CES
Andersson M. 1994. Sexual Selection. Princeton University Press, Princeton, New Jersey, USA.
Arbuthnott D, Elliot MG, McPeek MA & Crespi BJ. 2010. Divergent
patterns of diversification in courtship and genitalic characters of
Timema walking-sticks. Journal of Evolutionary Biology 23, 1399–
1411.
Arnold SJ & Wade MJ. 1984a. On the measurement of natural and sexual
selection: applications. Evolution 38, 720–734.
Arnold SJ & Wade MJ. 1984b. On the measurement of natural and sexual
selection: theory. Evolution 38, 709–719.
Arnqvist G. 1997. The evolution of animal genitalia: distinguishing
between hypotheses by single species studies. Biological Journal of
the Linnean Society 60, 365–379.
Arnqvist G. 1998. Comparative evidence for the evolution of genitalia by
sexual selection. Nature 393, 784–786.
Arnqvist G & Danielsson I. 1999. Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution 53,
147–156.
Arnqvist G & Rowe L. 1995. Sexual conflict and arms races between the
sexes: a morphological adaptation for control of mating in a female
insect. Proceedings of the Royal Society of London B 261, 123–127.
Arnqvist G & Rowe L. 2002. Correlated evolution of male and female
morphologies in water striders. Evolution 56, 936–947.
Arnqvist G & Rowe L. 2005. Sexual Conflict. Princeton University Press,
Princeton, New Jersey, USA.
Bath E, Tatarnic N & Bonduriansky R. 2012. Asymmetric reproductive
isolation and interference in neriid flies: the roles of genital morphology and behaviour. Animal Behaviour 84, 1331–1339.
Bertin A & Fairbairn DJ. 2005. One tool, many uses: precopulatory sexual
selection on genital morphology in Aquarius remigis. Journal of Evolutionary Biology 18, 949–961.
Bertin A & Fairbairn DJ. 2007. The form of sexual selection on male
genitalia cannot be inferred from within-population variance and
allometry – a case study in Aquarius remigis. Evolution 61, 825–837.
Blanckenhorn WU, Hosken DJ, Martin OY, Reim C, Teuschl Y & Ward
PI. 2002. The costs of copulating in the dung fly Sepsis cynipsea.
Behavioral Ecology 13, 353–358.
Blanckenhorn WU, Kraushaar URS, Teuschl Y & Reim C. 2004. Sexual
selection on morphological and physiological traits and fluctuating
asymmetry in the black scavenger fly Sepsis cynipsea. Journal of
Evolutionary Biology 17, 629–641.
Bonduriansky R. 2007. Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61, 838–849.
Bonduriansky R & Day T. 2003. The evolution of static allometry in
sexually selected traits. Evolution 57, 2450–2458.
Sexual selection and genital evolution
Brennan PLR, Prum RO, McCracken KG, Sorenson MD, Wilson RE &
Birkhead TR. 2007. Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2, e418.
Briceño RD & Eberhard W. 2009a. Experimental modifications imply a
stimulatory function for male tsetse fly genitalia, supporting cryptic
female choice theory. Journal of Evolutionary Biology 22, 1516–
1525.
Briceño RD & Eberhard WG. 2009b. Experimental demonstration of
possible cryptic female choice on male tsetse fly genitalia. Journal of
Insect Physiology 55, 989–996.
Brommer JE. 2011. Whither Pst? The approximation of Qst by Pst in
evolutionary and conservation biology. Journal of Evolutionary
Biology 24, 1160–1168.
Burns MM, Hedin M & Shultz JW. 2013. Comparative analyses of reproductive structures in harvestmen (Opiliones) reveal multiple transitions from courtship to precopulatory antagonism. PLoS ONE 8,
e66767.
Castellano S & Cermelli P. 2006. Reconciling sexual selection to species
recognition: a process-based model of mating decision. Journal of
Theoretical Biology 242, 529–538.
Cayetano L, Maklakov AA, Brooks RC & Bonduriansky R. 2011. Evolution of male and female genitalia following release from sexual selection. Evolution 65, 2171–2183.
Córdoba-Aguilar A. 1999. Male copulatory sensory stimulation induces
female ejection of rival sperm in a damselfly. Proceedings of the
Royal Society of London B 266, 779–784.
Córdoba-Aguilar A. 2002. Sensory trap as the mechanism of sexual selection in a damselfly genitalic trait (Insecta: Calopterygidae). American
Naturalist 160, 594–601.
Córdoba-Aguilar A. 2005. Possible coevolution of male and female
genital form and function in a calopterygid damselfly. Journal of
Evolutionary Biology 18, 132–137.
Córdoba-Aguilar A. 2009. Seasonal variation in genital and body size,
sperm displacement ability, female mating rate, and male harassment
in two calopterygid damselflies (Odonata: Calopterygidae). Biological Journal of the Linnean Society 96, 815–829.
Crudgington HS & Siva-Jothy MT. 2000. Genital damage, kicking and
early death. Nature 407, 855–856.
Danielsson I & Askenmo C. 1999. Male genital traits and mating interval
affect male fertilization success in the water strider Gerris lacustris.
Behavioral Ecology and Sociobiology 46, 149–156.
Dirsh VM. 1956. The phalic complex in Acridoidea (Orthoptera) in relation to taxonomy. Transactions of the Royal Entomological Society of
London 108, 223–356.
Dreyer AP & Shingleton AW. 2011. The effect of genetic and environmental variation on genital size in male Drosophila: canalized but
developmentally unstable. PLoS ONE 6, e28278.
Dufour L. 1848. Anatomie générale des Dipteres. Annuare de Science
Naturelle 1, 244–264.
Eberhard W. 2006. Sexually antagonistic coevolution in insects is associated with only limited morphological diversity. Journal of Evolutionary Biology 19, 657–681.
Eberhard W. 2009. Static allometry and animal genitalia. Evolution 63,
48–66.
Eberhard W. 2010. Evolution of genitalia: theories, evidence, and new
directions. Genetica 138, 5–18.
Eberhard WG. 1985. Sexual Selection and Animal Genitalia. Harvard
University Press, Cambridge, Massachusetts, USA.
Eberhard WG. 1996. Female Control: Sexual Selection by Cryptic
Female Choice. Princeton University Press, Princeton, New Jersey,
USA.
Eberhard WG. 2004a. Male–female conflict and genitalia: failure to
confirm predictions in insects and spiders. Biological Reviews 79,
121–186.
Eberhard WG. 2004b. Rapid divergent evolution of sexual morphology:
comparative tests of antagonistic coevolution and traditional female
choice. Evolution 58, 1947–1970.
Eberhard WG, Huber BA, Rodriguez RLS, Briceño RD, Salas I &
Rodriguez V. 1998. One size fits all? Relationships between the size
and degree of variation in genitalia and other body parts in twenty
species of insects and spiders. Evolution 52, 415–431.
15
Edelaar PIM, Burraco P & Gomez-Mestre I. 2011. Comparisons between
QST and FST—how wrong have we been? Molecular Ecology 20,
4830–4839.
Endler JA. 1989. Conceptual and other problems in speciation. In: Speciation and Its Consequences (eds D Otte & JA Endler), pp. 625–648.
Sinauer, Sunderland, Massachusetts, USA.
Endler JA & Houde AE. 1995. Geographic variation in female preferences
for male traits in Poecilia reticulata. Evolution 49, 456–468.
Evans JP, Gasparini C, Holwell GI, Ramnarine IW, Pitcher TE & Pilastro
A. 2011. Intraspecific evidence from guppies for correlated patterns of
male and female genital trait diversification. Proceedings of the Royal
Society of London B 278, 2611–2620.
Eyer JR. 1924. The comparative morphology of the male genitalia of the
primitive Lepidoptera. Annals of the Entomological Society of
America 17, 275–328.
Fairbairn DJ, Vermette R, Kapoor NN & Zahiri N. 2003. Functional
morphology of sexually selected genitalia in the water strider
Aquarius remigis. Canadian Journal of Zoology 81, 400–413.
Fricke C, Perry JC, Chapman T & Rowe L. 2009. The conditional economics of sexual conflict. Biology Letters 5, 671–674.
Gagnon MC & Turgeon J. 2011. Sexual conflict in Gerris gillettei (Insecta:
Hemiptera): intraspecific intersexual correlated morphology and
experimental assessment of behaviour and fitness. Journal of Evolutionary Biology 24, 1505–1516.
Grieshop K & Polak M. 2012. The precopulatory function of male genital
spines in Drosophila ananassae [doleschall] (diptera: drosophilidae)
revealed by laser surgery. Evolution 66, 2637–2645.
Higgie M & Blows MW. 2007. Are traits that experience reinforcement
also under sexual selection? American Naturalist 170, 409–420.
Holwell G. 2008. Geographic variation in genital morphology of
Ciulfina praying mantids. Journal of Zoology (London) 276, 108–
114.
Holwell G, Winnick C, Tregenza T & Herberstein ME. 2010. Genital
shape correlates with sperm transfer success in the praying mantis
Ciulfina klassi (Insecta: Mantodea). Behavioral Ecology and Sociobiology 64, 617–625.
Holwell GI & Herberstein ME. 2010. Chirally dimorphic male genitalia in
praying mantids (Ciulfina: Liturgusidae). Journal of Morphology 271,
1176–1184.
Hosken DJ, Minder AM & Ward PI. 2005. Male genital allometry in
Scathophagidae (Diptera). Evolutionary Ecology 19, 501–515.
Hosken DJ & Stockley P. 2004. Sexual selection and genital evolution.
Trends in Ecology and Evolution 19, 87–93.
Hotzy C, Polak M, Rönn JL & Arnqvist G. 2012. Phenotypic engineering
unveils the function of genital morphology. Current Biology 22,
2258–2261.
House CM, Lewis Z, Hodgson DJ et al. 2013. Sexual and natural selection
both influence male genital evolution. PLoS ONE 8, e63807.
House CM & Simmons LW. 2003. Genital morphology and fertilization
success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proceedings of the Royal Society of
London B 270, 447–455.
House CM & Simmons LW. 2007. No evidence for condition-dependent
expression of male genitalia in the dung beetle Onthophagus taurus.
Journal of Evolutionary Biology 20, 1322–1332.
Ilango K & Lane RP. 2000. Coadaptation of male aedeagal filaments and
female spermathecal ducts of the old world phlebotomine sand flies.
Journal of Medical Entomology 37, 653–659.
Jagadeeshan S & Singh RS. 2006. A time-sequence functional analysis of
mating behaviour and genital coupling in Drosophila: role of cryptic
female choice and male sex-drive in the evolution of male genitalia.
Journal of Evolutionary Biology 19, 1058–1070.
Kamimura Y. 2012. Correlated evolutionary changes in Drosophila
female genitalia reduce the possible infection risk caused by male
copulatory wounding. Behavioral Ecology and Sociobiology 66,
1107–1114.
Kamimura Y & Polak M. 2011. Does surgical manipulation of Drosophila
intromittent organs affect insemination success? Proceedings of the
Royal Society of London B 278, 815–816.
Kawano K. 2002. Character displacement in giant rhinoceros beetles.
American Naturalist 159, 255–271.
© 2013 Australian Entomological Society
16
L W Simmons
Kawano K. 2003. Character displacement in stag beetles (Coleoptera:
Lucanidae). Annals of the Entomological Society of America 96, 503–
511.
Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I & Whitlock M. 2012.
Experimental evolution. Trends in Ecology and Evolution 27, 547–
560.
Koshio C, Muraji M, Tatsuta H & Kudo S. 2007. Sexual selection in a
moth: effect of symmetry on male mating success in the wild.
Behavioral Ecology 18, 571–578.
Kuntner M, Coddington JA & Schneider JM. 2009. Intersexual arms race?
Genital coevolution in Nephilid spiders (Araneae, Nephilidae). Evolution 63, 1451–1463.
Lamy J-B, Plomion C, Kremer A & Delzon S. 2012. QST < FST as a
signature of canalization. Molecular Ecology 21, 5646–5655.
Lande R & Arnold SJ. 1983. The measurement of selection on correlated
characters. Evolution 37, 1210–1226.
van Lieshout E. 2011. Male genital length and mating status differentially
affect mating behaviour in an earwig. Behavioral Ecology and Sociobiology 65, 149–156.
van Lieshout E & Elgar MA. 2011. Longer exaggerated male genitalia
confer defensive sperm-competitive benefits in an earwig. Evolutionary Ecology 25, 351–362.
Lloyd JE. 1979. Mating behavior and natural selection. Florida Entomologist 62, 17–34.
Losos JB. 1999. Uncertainty in the reconstruction of ancestral character
states and limitations on the use of phylogenetic comparative
methods. Animal Behaviour 58, 1319–1324.
Macagno ALM, Pizzo A, Parzer HF, Palestrini C, Rolando A & Moczek
AP. 2011. Shape – but not size – codivergence between male and
female copulatory structures in Onthophagus Beetles. PLoS ONE 6,
e2889.
Márquez EJ & Knowles LL. 2007. Correlated evolution of multivariate
traits: detecting co-divergence across multiple dimensions. Journal of
Evolutionary Biology 20, 2334–2348.
Mayr E. 1963. Animal Species and Evolution. Harvard University Press,
Cambridge, Massachusetts, USA.
McKay JK & Latta RG. 2002. Adaptive population divergence: markers,
QTL and traits. Trends in Ecology and Evolution 17, 285–291.
McPeek MA, Shen L & Farid H. 2009. The correlated evolution of threedimensional reproductive structures between male and female damselflies. Evolution 63, 73–83.
McPeek MA, Shen L, Torrey JZ & Farid H. 2008. The tempo and mode of
three-dimensional morphological evolution in male reproductive
structures. American Naturalist 171, E158–E178.
Merilä J & Crnokrak P. 2001. Comparison of genetic differentiation at
marker loci and quantitative traits. Journal of Evolutionary Biology
14, 892–903.
Moreno-Garcia M & Cordero C. 2008. On the function of male genital
claspers in Stenomacra marginella (Heteroptera: Largidae). Journal
of Ethology 26, 255–260.
Nagata N, Kubota K, Takami Y & Sota T. 2009. Historical divergence of
mechanical isolation agents in the ground beetle Carabus arrowianus
as revealed by phylogeographical analyses. Molecular Ecology 18,
1408–1421.
Otronen M. 1998. Male asymmetry and postcopulatory sexual selection in
the fly Dryomyza anilis. Behavioral Ecology and Sociobiology 42,
185–192.
Parker GA. 1979. Sexual selection and sexual conflict. In: Sexual Selection and Reproductive Competition in Insects (eds MS Blum & NA
Blum), pp. 123–166. Academic Press, London, UK.
Patterson BD & Thaeler CS. 1982. The mammalian baculum: hypotheses
on the nature of bacular variability. Journal of Mammalogy 63, 1–15.
Perry JC & Rowe L. 2012. Sexual conflict and antagonistic coevolution
across water strider populations. Evolution 66, 544–557.
Petrie M. 1988. Intraspecific variation in structures that display competitive ability: large animals invest relatively more. Animal Behaviour
36, 1174–1180.
Phillips PC & Arnold SJ. 1989. Visualizing multivariate selection. Evolution 43, 1209–1222.
Pizzo A, Roggero A, Palestrini C, Moczek AP & Rolando A. 2008. Rapid
shape divergences between natural and introduced populations of a
© 2013 Australian Entomological Society
horned beetle partly mirror divergences between species. Evolution
and Development 10, 166–175.
Polak M & Rashed A. 2010. Microscale laser surgery reveals adaptive
function of male intromittent genitalia. Proceedings of the Royal
Society of London B 277, 1371–1376.
Polihronakis M. 2006. Morphometric analysis of intraspecific shape variation in male and female genitalia of Phyllophaga hirticula
(Coleoptera: Scarabaeidae: Melolonthinae). Annals of the Entomological Society of America 99, 144–150.
Polihronakis M. 2009. Hierarchical comparative analysis of genetic and
genitalic geographical structure: testing patterns of male and female
genital evolution in the scarab beetle Phyllophaga hirticula
(Coleoptera: Scarabaeidae). Biological Journal of the Linnean Society
96, 135–149.
Preziosi RF & Fairbairn DJ. 2000. Lifetime selection on adult body size
and components of body size in a waterstrider: opposing selection and
maintenance of sexual size dimorphism. Evolution 54, 558–566.
Puniamoorthy N, Kotrba M & Meier R. 2010. Unlocking the ‘Black box’:
internal female genitalia in Sepsidae (Diptera) evolve fast and are
species-specific. BMC Evolutionary Biology 10, 275.
Richards OW. 1927a. Sexual selection and related problems in the insects.
Biological Reviews 2, 298–364.
Richards OW. 1927b. The specific characters of British bumblebees
(Hymenoptera). Transactions of the Royal Entomological Society of
London 75, 233–265.
Richmond MP, Johnson S & Markow TA. 2012. Evolution of reproductive
morphology among recently diverged taxa in the Drosophila
mojavensis species cluster. Ecology and Evolution 2, 397–408.
Ritchie MG. 2007. Sexual selection and speciation. Annual Review of
Ecology, Evolution, and Systematics 38, 79–102.
Robinson JV & Novak KL. 1997. The relationship between mating system
and penis morphology in ischnuran damselflies (Odonata:
Coenagrionidae). Biological Journal of the Linnean Society 60, 187–
200.
Rodriguez V. 1995. Relation of flagellum length to reproductive success in
male Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae:
Cassidinae). Coleopterists’ Bulletin 49, 201–205.
Rodriguez V, Windsor D & Eberhard WG. 2004. Tortoise beetle genitalia
and demonstrations of a sexually selected advantage for flagellum
length in Chelymorpha alternans (Chrysomelidae, Cassidini, Stolaini.
In: New Developments in the Biology of Chrysomelidae (eds P Jolivet,
JA Santiago-Blay & M Schmitt), pp. 739–748. SPB Academic Publishing, The Hague, Netherlands.
Rodríguez RL & Al-Wathiqui N. 2011. Genotype x environment interaction is weaker in genitalia than in mating signals and body traits in
Enchenopa treehoppers (Hemiptera: Membracidae). Genetica 139,
871–884.
Rodríguez RL & Al-Wathiqui N. 2012. Genotype × environment interaction in the allometry of body, genitalia and signal traits in Enchenopa
treehoppers (Hemiptera: Membracidae). Biological Journal of the
Linnean Society 105, 187–196.
Roig-Alsina A. 1993. The evolution of the apoid endophallus, its
phylogenetic implications, and functional significance of the genital
capsule (Hymenoptera, Apoidea). Bollettino di Zoologia 60, 169–183.
Rönn J, Katvala M & Arnqvist G. 2007. Coevolution between harmful
male genitalia and female resistance in seed beetles. Proceedings of
the National Academy of Sciences of the United States of America
104, 10921–10925.
Rowe L. 1994. The costs of mating and mate choice in water striders.
Animal Behaviour 48, 1049–1056.
Rowe L & Arnqvist G. 2012. Sexual selection and the evolution of genital
shape and complexity in water striders. Evolution 66, 40–54.
Ryan MJ & Rand AS. 1993. Species recognition and sexual selection as a
unitary problem in animal communication. Evolution 47, 647–657.
Sakurai G, Himuro C & Kasuya E. 2012. Intra-specific variation in the
morphology and the benefit of large genital sclerites of males in the
adzuki bean beetle (Callosobruchus chinensis). Journal of Evolutionary Biology 25, 1291–1297.
Sánchez V, Hernández-Baños BE & Cordero C. 2011. The evolution of a
female genital trait widely distributed in the lepidoptera: comparative
evidence for an effect of sexual coevolution. PLoS ONE 6, e22642.
Sexual selection and genital evolution
Sasabe M, Takami Y & Sota T. 2010. QTL for the species-specific male
and female genital morphologies in Ohomopterus ground beetles.
Molecular Ecology 19, 5231–5239.
Shapiro AM & Porter AH. 1989. The lock-and-key hypothesis: evolutionary and biosystematic interpretation of insect genitalia. Annual
Review of Entomology 34, 231–245.
Simmons LW. 2001. Sperm Competition and Its Evolutionary Consequences in the Insects. Princeton University Press, Princeton, New
Jersey, USA.
Simmons LW, Beveridge M & Krauss S. 2004. Genetic analysis of parentage within experimental populations of a male dimorphic beetle,
Onthophagus taurus, using amplified fragment length polymorphism.
Behavioral Ecology and Sociobiology 57, 164–173.
Simmons LW & Fitzpatrick JL. 2012. Sperm wars and the evolution of
male fertility. Reproduction 144, 519–534.
Simmons LW & García-González F. 2008. Evolutionary reduction in
testes size and competitive fertilization success in response to the
experimental removal of sexual selection in dung beetles. Evolution
62, 2580–2591.
Simmons LW & Garcia-Gonzalez F. 2011. Experimental coevolution of
male and female genital morphology. Nature Communications 2, 374.
doi:10.1038/ncomms1379
Simmons LW & Holley R. 2011. Offspring viability benefits but no apparent costs of mating with high quality males. Biology Letters 7, 419–
421.
Simmons LW, House CM, Hunt J & García-González F. 2009. Evolutionary response to sexual selection in male genital morphology. Current
Biology 19, 1442–1446.
Simmons LW & Tomkins JL. 1996. Sexual selection and the allometry of
earwig forceps. Evolutionary Ecology 10, 97–104.
Song H & Bucheli SR. 2010. Comparison of phylogenetic signal between
male genitalia and non-genital characters in insect systematics.
Cladistics 26, 23–35.
Sota T & Kubota K. 1998. Genital lock-and-key as a selective agent
against hybridization. Evolution 52, 1507–1513.
Soulier-Perkins A. 2001. The phylogeny of the Lophopidae and the impact
of sexual selection and coevolutionary sexual conflict. Cladistics 17,
56–78.
Tadler A. 1999. Selection of a conspicuous male genitalic trait in seedbug
Lygaeus simulans. Proceedings of the Royal Society of London B 266,
1773–1777.
Tadler A & Nemeschkal HL. 1999. Selection of male traits during and
after copulation in the seedbug Lygaeus simulans (Heteroptera,
Lygaeidae). Biological Journal of the Linnean Society 68, 471–483.
Takami Y. 2003. Experimental analysis of the effect of genital morphology on insemination success in the ground beetle Carabus insulicola.
Ethology Ecology and Evolution 15, 51–61.
Takami Y & Soto T. 2007. Rapid diversification of male genitalia and
mating strategies in Ohomopterus ground beetles. Journal of Evolutionary Biology 20, 1385–1395.
Tarasov SI & Solodovnikov AY. 2011. Phylogenetic analyses reveal
reliable morphological markers to classify mega-diversity in
17
Onthophagini dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae).
Cladistics 27, 1–39.
Tatarnic NJ & Cassis G. 2010. Sexual coevolution in the traumatically
inseminating plant bug genus Coridromius. Journal of Evolutionary
Biology 23, 1321–1326.
Thornhill R & Alcock J. 1983. The Evolution of Insect Mating Systems.
Harvard University Press, Cambridge, Massachusetts, USA.
Tsuchiya K & Hayashi F. 2008. Surgical examination of male genital
function of calopterygid damselflies (Odonata). Behavioral Ecology
and Sociobiology 62, 1417–1425.
Tuxen SL. 1970. Taxonomists Glossary of Genitalia in Insects. Scandinavian University Press, Copenhagen, Denmark.
Vahed K, Lehmann AW, Gilbert JDJ & Lehmann GUC. 2011. Increased
copulation duration before ejaculate transfer is associated with larger
spermatophores, and male genital titillators, across bushcricket taxa.
Journal of Evolutionary Biology 24, 1960–1968.
Waage JK. 1979. Dual function of the damselfly penis: sperm removal and
transfer. Science 203, 916–918.
Wenninger EJ & Averill AL. 2006. Influence of body and genital morphology on relative male fertilization success in oriental beetle.
Behavioral Ecology 17, 656–663.
Werner M & Simmons LW. 2008. The evolution of male genitalia:
functional integration of genital sclerites in the dung beetle
Onthophagus taurus. Biological Journal of the Linnean Society
93, 257–266.
Whitlock MC. 2008. Evolutionary inference from QST. Molecular
Ecology 17, 1885–1896.
Wilkinson GS. 1993. Artificial sexual selection alters allometry in the
stalk-eyed fly Cyrtodiopsis dalmanni (Diptera: Diopsidae). Genetical
Research 62, 213–222.
Wilkinson GS & Taper M. 1999. Evolution of genetic variation for
condition-dependent traits in stalk-eyed flies. Proceedings of the
Royal Society of London B 266, 1685–1690.
Wojcieszek JM, Austin P, Harvey MS & Simmons LW. 2012. Micro-CT
scanning provides insight into the functional morphology of millipede
genitalia. Journal of Zoology 287, 91–95.
Wojcieszek JM & Simmons LW. 2012. Evidence for stabilizing selection
and slow divergent evolution of male genitalia in a millipede
(Antichiropus variabilis). Evolution 66, 1138–1153.
Wojcieszek JM & Simmons LW. 2013. Divergence in genital morphology
may contribute to mechanical reproductive isolation in a millipede.
Ecology and Evolution 3, 334–343.
Xu J & Wang Q. 2010. Form and nature of precopulatory sexual selection
in both sexes of a moth. Naturwissenschaften 97, 617–625.
Yassin A & Orgogozo V. 2013. Coevolution between male and female
genitalia in the Drosophila melanogaster species subgroup. PLoS
ONE 8, e57158.
Zunino M. 1979. Gruppi artificiali e gruppi naturali negli Onthophagus
(Coleoptera, Scarabaeoidea). Bollettino dei Musei di Zoologia e
Anatomia comparata, Torino 1, 1–18.
Accepted for publication 10 July 2013.
© 2013 Australian Entomological Society