Mosaic pattern of genital divergence in three populations of Schistocerca lineata Scudder, 1899 (Orthoptera: Acrididae: Cyrtacanthacridinae)

Sexual selection theory predicts that genital structures in isolated populations are likely to diverge, but male genitalia are often species-specific, which led to the idea that male genitalia are relatively invariable within species. Previous allometric studies collectively suggested that male genitalia are intraspecifically invariable in size compared with external body parts. We investigated whether male genitalia are invariable in shape in three populations of a grasshopper Schistocerca lineata Scudder, 1899, using two independent methods of geometric morphometric analyses. Specifically, we focused on the idea that male genitalia are complex structures consisting of many functionally different components, and studied how these individual parts diverge among three populations. Individual components of male genitalia show different population-level divergence, resulting in the mosaic pattern of genital divergence. Individual components diverge independently from each other. Body size is positively correlated with genitalia size, but is significantly correlated with the shape of only one of the three genital structures we measured. Thus, different components of male genitalia may be influenced by different evolutionary processes. This study is the first to show that components of complex genitalia evolve separately within a species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 289–301.     

Shape--but not size--codivergence between male and female copulatory structures in Onthophagus beetles

Genitalia are among the fastest evolving morphological traits in arthropods. Among the many hypotheses aimed at explaining this observation, some explicitly or implicitly predict concomitant male and female changes of genital traits that interact during copulation (i.e., lock and key, sexual conflict, cryptic female choice and pleiotropy). Testing these hypotheses requires insights into whether male and female copulatory structures that physically interact during mating also affect each other's evolution and patterns of diversification. Here we compare and contrast size and shape evolution of male and female structures that are known to interact tightly during copulation using two model systems: (a) the sister species O. taurus (1 native, 3 recently established populations) and O. illyricus, and (b) the species-complex O. fracticornis-similis-opacicollis. Partial Least Squares analyses indicated very little to no correlation between size and shape of copulatory structures, both in males and females. Accordingly, comparing shape and size diversification patterns of genitalia within each sex showed that the two components diversify readily--though largely independently of each other--within and between species. Similarly, comparing patterns of divergence across sexes showed that relative sizes of male and female copulatory organs diversify largely independent of each other. However, performing this analysis for genital shape revealed a signature of parallel divergence. Our results therefore suggest that male and female copulatory structures that are linked mechanically during copulation may diverge in concert with respect to their shapes. Furthermore, our results suggest that genital divergence in general, and co-divergence of male and female genital shape in particular, can evolve over an extraordinarily short time frame. Results are discussed in the framework of the hypotheses that assume or predict concomitant evolutionary changes in male and female copulatory organs.     

BOTH MALE AND FEMALE NOVEL TRAITS PROMOTE THE CORRELATED EVOLUTION OF GENITALIA BETWEEN THE SEXES IN AN ARTHROPOD

The correlated evolution of genitalia between sexes has been demonstrated in many taxa. However, it remains unclear whether female rather than male genitalia can play a key role in the correlated evolution of male and female genitalia. We conducted an extensive cross‐population analysis of the divergence patterns of genital structures, weights of whole genital organs, and the bodies of both sexes, and male genital length in a group of xystodesmid millipedes showing diverse genital morphologies. We demonstrate that the correlated evolution of male and female genitalia toward exaggerated states has occurred in the millipedes, which have evolved novel traits in both males (forceps‐like gonopods) and females (retractable bellows). Enlargement and elongation of forceps‐like gonopods may be advantageous in sperm competition, whereas enlargement and elongation of the bellows may facilitate acceptance/rejection of insemination for ensuring the female's fitness. These male and female genital parts have affected the correlated evolution in the opposite sex, resulting in diversification and exaggeration of genital morphology. Our study suggests that evolutionary novel traits in not only males but also in females could play an important role in the correlated evolution of genitalia between the sexes.     

Molecular phylogeny reveals the repeated evolution of complex male genital traits in the New Zealand moth genus Izatha (Lepidoptera: Xyloryctidae)

Male genitalia are among the most rapidly evolving and divergent morphological structures and sexual selection is known to drive this phenomenon in many taxa. Because of their diversity, even within a single genus, genital characters are frequently used to infer relationships among closely‐related species. Moths within the genus Izatha (Xyloryctidae) are ideal candidates for investigating the phylogenetic patterns of genital evolution as they display great variation in male genital structure and complexity. We determined the evolutionary relationships among 31 species of Izatha by constructing a molecular phylogeny of the genus based on the mitochondrial cytochrome oxidase subunit I gene and the isocitrate dehydrogenase and carbamoylphosphate synthase domain protein nuclear genes. This allowed estimations of ancestral male genital character states and patterns of male genital diversification using maximum‐likelihood models. The genus is divided into two well‐supported clades and two poorly supported clades at the root of the phylogeny with incomplete phylogenetic resolution within two species groups, likely due to rapid speciation. Izatha display a number of apomorphic phallic traits including cornuti (sclerotized spines) which are either discharged into the female during copulation (deciduous cornuti) or fixed to the male phallus (compound and fish‐hook cornuti). Within the genus, there is a reduction of secondary genital characters – the uncus and gnathos – but an elaboration of another grasping structure, the juxta; the potential origin and functionality of these male genital traits are discussed. Overall, some male genital characters provided a good indication of species relationships; however, several parts of the complex male genitalia of Izatha show evidence of homoplasy and convergence highlighting the problems of using these traits in determining species relationships. Additionally, this convergence has highlighted that complex genital structures may evolve repeatedly and independently within a lineage.     

Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating

Natural selection and post‐copulatory sexual selection, including sexual conflict, contribute to genital diversification. Fundamental first steps in understanding how these processes shape the evolution of specific genital traits are to determine their function experimentally and to understand the interactions between female and male genitalia during copulation. Our experimental manipulations of male and female genitalia in red‐sided garter snakes (Thamnophis sirtalis parietalis) reveal that copulation duration and copulatory plug deposition, as well as total and oviductal/vaginal sperm counts, are influenced by the interaction between male and female genital traits and female behaviour during copulation. By mating females with anesthetized cloacae to males with spine‐ablated hemipenes using a fully factorial design, we identified significant female–male copulatory trait interactions and found that females prevent sperm from entering their oviducts by contracting their vaginal pouch. Furthermore, these muscular contractions limit copulatory plug size, whereas the basal spine of the male hemipene aids in sperm and plug transfer. Our results are consistent with a role of sexual conflict in mating interactions and highlight the evolutionary importance of female resistance to reproductive outcomes.     

Evidence for stabilizing selection and slow divergent evolution of male genitalia in a millipede (Antichiropus variabilis)

It is generally accepted that postcopulatory sexual selection drives rapid divergence of genital morphology among isolated populations. The mode of selection operating upon genitalia can be explored by comparing patterns of population divergence in genetic and genitalic traits. We collected Antichiropus variabilis millipedes from eight localities across the species range. Levels of among-population genetic divergence, at microsatellite loci, and the mitochondrial COI gene were very high. Following geometric morphometric analyses, genital morphology was also found to be highly divergent among the populations surveyed, whereas head morphology had not diverged as markedly. However, pairwise comparisons of F(ST) and P(ST) showed that among-population divergence in both genital and head shape was significantly lower than that experienced by neutral genetic markers. Our results suggest that the genitalia of A. variabilis are currently experiencing a period of stabilizing selection, the mode of selection expected for genitalia that function in species recognition via a "lock-and-key" mechanism. Our results demonstrate that although genital morphology can clearly diverge among genetically isolated populations, divergence is not necessarily as rapid as commonly argued, and continuous directional sexual selection may not always underpin the evolutionary divergence of male genitalia.     

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, and fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H₂S containing) and nearby nonsulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation‐with‐gene‐flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.     

Sexual selection and the evolution of genital shape and complexity in water striders

Animal genitalia show two striking but incompletely understood evolutionary trends: a great evolutionary divergence in the shape of genitalic structures, and characteristic structural complexity. Both features are thought to result from sexual selection, but explicit comparative tests are hampered by the fact that it is difficult to quantify both morphological complexity and divergence in shape. We undertake a comparative study of multiple nongenitalic and male genital traits in a clade of 15 water strider species to quantify complexity and shape divergence. We show that genital structures are more complex and their shape more divergent among species than nongenital traits. Further, intromittent genital traits are more complex and have evolved more divergently than nonintromittent genital traits. More importantly, shape and complexity of nonintromittent genital traits show correlated evolution with indices of premating sexual selection and intromittent genital traits with postmating sexual selection, suggesting that the evolution of different components of genital morphology are shaped independently by distinct forms of sexual selection. Our quantitative results provide direct comparative support for the hypothesis that sexual selection is associated with morphological complexity in genitalic traits and highlight the importance of quantifying morphological shape and complexity, rather than size in studies of genital evolution.     

A statistical framework for testing modularity in multidimensional data

Modular variation of multivariate traits results from modular distribution of effects of genetic and epigenetic interactions among those traits. However, statistical methods rarely detect truly modular patterns, possibly because the processes that generate intramodular associations may overlap spatially. Methodologically, this overlap may cause multiple patterns of modularity to be equally consistent with observed covariances. To deal with this indeterminacy, the present study outlines a framework for testing a priori hypotheses of modularity in which putative modules are mathematically represented as multidimensional subspaces embedded in the data. Model expectations are computed by subdividing the data into arrays of variables, and intermodular interactions are represented by overlapping arrays. Covariance structures are thus modeled as the outcome of complex and nonorthogonal intermodular interactions. This approach is demonstrated by analyzing mandibular modularity in nine rodent species. A total of 620 models are fit to each species, and the most strongly supported are heuristically modified to improve their fit. Five modules common to all species are identified, which approximately map to the developmental modules of the mandible. Within species, these modules are embedded within larger "super-modules," suggesting that these conserved modules act as building blocks from which covariation patterns are built.     

Copulatory mechanism in a sexually cannibalistic spider with genital mutilation (Araneae: Araneidae: Argiope bruennichi)

Genitalia are among the fastest evolving morphological traits as evidenced by their common function as diagnostic traits in species identification. Even though the main function of genitalia is the successful transfer of spermatozoa, the presence of diverse structures that are obviously not necessary for this suggests that genitalia are a target of sexual selection. The male genitalia of many spider species are extremely complex and equipped with numerous sclerites, plates and spines whose functions are largely unknown. Selection on male genitalia may be particularly strong in sexually cannibalistic spiders, where mating success of males is restricted to a single female. We investigated the copulatory mechanism of the sexually cannibalistic orb weaving spider Argiope bruennichi by shock freezing mating pairs and revealed a complicated interaction between the appendices and sclerites that make up the male gonopods (paired pedipalps). The plate that covers the female genital opening (scape) is secured between two appendices of the male genital bulb, while three sclerites that bear the sperm duct are unfolded and extended into the female copulatory opening. During copulation, females attack and cannibalise the male and males mutilate their genitalia in about 80% of cases. Our study demonstrates that (i) genital coupling is largely accomplished on the external part of the female genitalia, (ii) that the mechanism requires an interaction between several non-sperm-transferring structures and (iii) that there are two predetermined breaking points in the male genitalia. Further comparative work on the genus Argiope will test if the copulatory mechanism with genital mutilation indeed is an adaptation to sexual cannibalism or if cannibalism is a female counter adaptation to male monopolisation through genital plugging.     

Bat genitalia: allometry, variation and good genes

Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 497–507.     

Coevolution of male and female reproductive structures in Drosophila

The morphology of male genitalia whilst stable within species, exhibits huge interspecific variation. This variation is likely to be as a result of sexual selection due to the direct involvement of these reproductive structures in mating and sperm transfer. In contrast, internal soft tissue components of the genitalia are generally poorly investigated as they are not directly involved in physical and mechanical adequacy during sperm transfer. However, these soft tissue structures may also drive differential male–female interactions, particularly in internally fertilising organisms where females have the ability to store sperm and bias male reproductive success. In this paper we use the drosophila model to investigate the role of male and female reproductive elements in sexual selection. Our meta-analysis supplemented with additional new data clearly shows that within species, sperm length versus testis length, and sperm length versus seminal receptacle length, are highly correlated. Thus, independent of the phylogenetic relationship among species, gamete evolution is likely to result in sexual selection interactions that drive the evolution of internal reproductive components in both sexes. Our results and discussion of the literature highlight the importance of considering internal soft structures that may influence fertilisation, when investigating selective forces acting on the evolution of reproductive traits.     

The evolution of male genitalia: functional integration of genital sclerites in the dung beetle Onthophagus taurus

It is now widely recognized that sexual selection has been important in the rapid and divergent evolution of male genital morphology. However, distinguishing among putative mechanisms of sexual selection acting on male genital morphology represents a considerable challenge. Although there is growing evidence that variation in the size and/or shape of male genital structures can determine a male's success in gaining fertilizations, our knowledge of the functional morphology of male genitalia remains limited. Here we examine the functional morphology of genital sclerites that are known to influence paternity in the dung beetle Onthophagus taurus . We show that three of the sclerites form a functionally integrated unit that generates the tubular-shaped spermatophore and delivers its opening to the female's spermathecal duct. A fourth sclerite acts as a holdfast device during copulation. Our observations shed light on the mechanism by which these sclerites influence a male's paternity, and their patterns of phenotypic and genetic (co)variation.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 257–266.     

Distinctive developmental variability of genital parts in the sexually dimorphic beetle, Prosopocoilus inclinatus (Coleoptera: Lucanidae)

Recent comparative studies have revealed that the rapid diversity of genitalia is closely related to sexual selection and that genital development interacts with the development of different body parts. Hypotheses about developmental stability due to selection to genital parts were tested by estimating allometric relations in a sexually dimorphic stag beetle Prosopocoilus inclinatus . All genital parts of males scaled to body size with a slope of less than 1 and all but the median lobe (male intromittent organ) showed smaller variability than other body parts. This supported the 'one-size-fits-all' hypothesis, which suggests broad copulation opportunity by males of any size with females within a population. Nevertheless, we found large variation among different genital parts in coefficients of variation and in values of the switch point where the allometric relations varied significantly. These results strongly support the view that developmental trajectories of genital traits are not necessarily integrated. Among the genitalic traits, male intromittent organ and female genitalia exhibited large variability, suggesting a high responsiveness to the selective regimes and physical interaction during copulation. This may account for rapid diversification of genital morphology, even in closely-related populations in beetle species.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 573–581.     

Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia

The spectacular variability that typically characterizes male genital traits has largely been attributed to the role of sexual selection. Among the evolutionary mechanisms proposed to account for this diversity, two processes in particular have generated considerable interest. On the one hand, females may exploit postcopulatory mechanisms of selection to favour males with preferred genital traits (cryptic female choice; CFC), while on the other hand females may evolve structures or behaviours that mitigate the direct costs imposed by male genitalia (sexual conflict; SC). A critical but rarely explored assumption underlying both processes is that male and female reproductive traits coevolve, either via the classic Fisherian model of preference-trait coevolution (CFC) or through sexually antagonistic selection (SC). Here, we provide evidence for this prediction in the guppy (Poecilia reticulata), a polyandrous livebearing fish in which males transfer sperm internally to females via consensual and forced matings. Our results from a paternal half-sibling breeding design reveal substantial levels of additive genetic variation underlying male genital size and morphology—two traits known to predict mating success during non-consensual matings. Our subsequent finding that physically interacting female genital traits exhibit corresponding levels of genetic (co)variation reveals the potential intersexual coevolutionary dynamics of male and female genitalia, thereby fulfilling a fundamental assumption underlying CFC and SC theory.     

Experimental modifications imply a stimulatory function for male tsetse fly genitalia,supporting cryptic female choice theory

One of the most sweeping of all patterns in morphological evolution is that animal genitalia tend to diverge more rapidly than do other structures. Abundant indirect evidence supports the cryptic female choice (CFC) explanation of this pattern, which supposes that male genitalia often function to court females during copulation; but direct experimental demonstrations of a stimulatory function have been lacking. In this study, we altered the form of two male genital structures that squeeze the female’s abdomen rhythmically in Glossina pallidipes flies. As predicted by theory, this induced CFC against the male: ovulation and sperm storage decreased, while female remating increased. Further experiments showed that these effects were due to changes in tactile stimuli received by the female from the male’s altered genitalia, and were not due to other possible changes in the males due to alteration of their genital form. Stimulation from male genital structures also induces females to permit copulation to occur. Together with previous studies of tsetse reproductive physiology, these data constitute the most complete experimental confirmation that sexual selection (probably by CFC) acts on the stimulatory properties of male genitalia.     

The coevolution of male and female genitalia in a mammal: A quantitative genetic insight

Male genitalia are among the most phenotypically diverse morphological traits, and sexual selection is widely accepted as being responsible for their evolutionary divergence. Studies of house mice suggest that the shape of the baculum (penis bone) affects male reproductive fitness and experimentally imposed postmating sexual selection has been shown to drive divergence in baculum shape across generations. Much less is known of the morphology of female genitalia and its coevolution with male genitalia. In light of this, we used a paternal half-sibling design to explore patterns of additive genetic variation and covariation underlying baculum shape and female vaginal tract size in house mice (Mus musculus domesticus). We applied a landmark-based morphometrics approach to measure baculum size and shape in males and the length of the vaginal tract and width of the cervix in females. Our results reveal significant additive genetic variation in house mouse baculum morphology and cervix width, as well as evidence for genetic covariation between male and female genital measures. Our data thereby provide novel insight into the potential for the coevolutionary divergence of male and female genital traits in a mammal.     

Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

In contrast to male genitalia that typically exhibit patterns of rapid and divergent evolution among internally fertilizing animals, female genitalia have been less well studied and are generally thought to evolve slowly among closely-related species. As a result, few cases of male-female genital coevolution have been documented. In Drosophila, female copulatory structures have been claimed to be mostly invariant compared to male structures. Here, we re-examined male and female genitalia in the nine species of the D. melanogaster subgroup. We describe several new species-specific female genital structures that appear to coevolve with male genital structures, and provide evidence that the coevolving structures contact each other during copulation. Several female structures might be defensive shields against apparently harmful male structures, such as cercal teeth, phallic hooks and spines. Evidence for male-female morphological coevolution in Drosophila has previously been shown at the post-copulatory level (e.g., sperm length and sperm storage organ size), and our results provide support for male-female coevolution at the copulatory level.     

The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus

Three main hypotheses, have been invoked to explain divergent genital evolution, the lock and key, pleiotropy, and sexual selection hypotheses, each of which make different predictions about how genital traits are inherited. Here we used a half-sib breeding design to examine the patterns of genetic variation and covariation between male genital sclerites, and their covariance with general body morphology in the dung beetle Onthophagus taurus. We found CV(A)'s and CV(P)'s were similar for both genital and general morphological traits and that CV(R)'s were large for both trait types. We found that male genital sclerites were negatively genetically correlated with general morphological traits. Variation in male genital morphology has direct implications for a male's fertilization success and the resulting sexual selection acting on male genitalia is predicted to maintain high levels of additive genetic variance. Contrary to this prediction, we found that individual genital sclerites all had low levels of additive genetic variance and large maternal and environmental sources of variation. Our data suggest that the genital sclerites in O. taurus are not inherited independently but as a genetically integrated unit. More importantly, the way the different sclerites function to influence male fertilization success reflects this genetic integration. Even though levels of V(A) in individual genital sclerites may be low, there may still be sufficient V(A) in multivariate trait space for selection to generate evolutionary change in the overall morphology of male genitalia.