The functional morphology of species-specific clasping structures on the front legs of male Archisepsis and Palaeosepsis flies (Diptera, Sepsidae)

Several possible explanations for the elaborate species-specific morphology of male front leg clasping organs were tested by comparing six species of Archisepsis, Palaeosepsis and Microsepsis flies. The only previously published hypothesis regarding these clasping organs was refuted by the finding that species-specific portions of the male femur and tibia consistently meshed tightly with prominent veins and folds in the female's wing, rather than meshing with each other. Female wing morphology in the region grasped by the male was relatively uniform and in general did not vary in ways that would prevent non-conspecific males from grasping them, arguing in all but one species against both simple lock-and-key and male-female conflict of interests hypotheses based on morphology. Interspecific differences in male front leg morphology generally represent alternative ways to accomplish the same basic mechanical function of holding tightly onto the relatively invariant female. Despite the fact that female resistance behaviour indicates that male-female conflict over male mounting is common, only one female wing structure in one species resembled an anti-clasper device, giving a second reason to doubt the morphological male-female conflict of interest hypothesis, at least for five of the six species. The positions of probable sensory structures on the wings of females were relatively similar in different species and did not correspond in any obvious way to species-specific features of male clasping structures. This, plus the intraspecific variation in both the positions of these sensilla and the exact site where the male grasped the female's wing, argued against simple 'sensory lock-and-key' ideas about male front leg function. By a process of elimination, it appears that generalized female receptors are able to sense species-specific differences in male front legs. This idea was supported by increased female rejection behaviour in cross-specific pairs.     

Evolution of animal genitalia: morphological correlates of fitness components in a water strider

Rapid divergence of male genitalia is one of the most general evolutionary trends in animals with internal fertilization, but the mechanisms of genital evolution are poorly understood. The current study represents the first comprehensive attempt to test the main hypotheses that have been suggested to account for genital evolution (the lock-and-key, sexual selection and pleiotropy hypotheses) with intraspecific data. We measure multivariate phenotypic selection in a water strider species, by relating five different components of fitness (mating frequency, fecundity, egg hatching rate, offspring survival rate and offspring growth rate) to a suite of genital and non-genital morphological traits (in total 48). Body size had a series of direct effects in both sexes. Large size in females was positively related to both fecundity and egg hatching rate. There was positive sexual selection for large size in males (mating frequency), which to some extent was offset by a reduced number of eggs laid by females mated to large males. Male genitalic morphology influenced male mating frequency, but the detected directional selection on genitalia was due to indirect selection on phenotypically correlated non-intromittent traits. Further, we found no assortative mating between male intromittent genitalia and female morphology. Neither did we find any indications of male genitalia conveying information of male genetic quality. Several new insights can be gained from our study. Most importantly, our results are in stark disagreement with the long standing lock-and-key hypothesis of genital evolution, as well as with certain models of sexual selection. Our results are, however, in agreement with other models of sexual selection as well as with the pleiotropy hypothesis of genital evolution. Fluctuating asymmetry of bilaterally symmetrical traits, genital as well as non-genital, had few effects on fitness. Females with low fluctuating asymmetry in leg length produced offspring with a higher survival rate, a pattern most proba bly caused by direct phenotypic maternal effects. We also discuss the relevance of our results to sexual conflict over mating, and the evolution of sexual traits by coevolutionary arms races between the sexes.     

Species-specific genitalic copulatory courtship in sepsid flies (Diptera, Sepsidae, Microsepsis) and theories of genitalic evolution

Males of Microsepsis eberhardi and M. armillata use their genitalic surstyli to rhythmically squeeze the female's abdomen with stereotyped movements during copulation. Squeezing movements did not begin until intromission had occurred and, contrary to predictions of the conflict-of-interest hypothesis for genitalic evolution, did not overcome morphological or behavioral female resistance. Contrary to predictions of the lock-and-key hypothesis, female morphology was uniform in the two species and could not mechanically exclude the genitalia of either species of male. The complex pattern of squeezing movements differed between the two species as predicted by the sexual selection hypothesis for genitalic evolution. Also, evolutionarily derived muscles and pseudoarticulations in the male's genitalic surstyli facilitated one type of movement, whose patterns were especially distinct. The data support the hypothesis that the male surstyli evolved to function as courtship devices.     

Sex allocation and sexual conflict in simultaneously hermaphroditic animals

Links between sex allocation (SA) and sexual conflict in simultaneous hermaphrodites have been evident since Charnov''s landmark paper published 30 years ago. We discuss two links, namely the potential for sexual conflict over SA between sperm donor and recipient, and the importance of post-copulatory sexual selection and the resulting sexual conflict for the evolution of SA. We cover the little empirical and theoretical work exploring these links, and present an experimental test of one theoretical prediction. The link between SA and sexual conflict is an interesting field for future empirical and theoretical research.     

Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice

Male structures specialized to contact females during sexual interactions often diverge relatively rapidly over evolutionary time. Previous explanations for this pattern invoked sexual selection by female choice, but new ideas emphasize possible sexually antagonistic coevolution resulting from male-female conflict over control of fertilization. The two types of selection have often not been carefully distinguished. They do not theoretically exclude one another, but they have not necessarily had equally important roles in producing rapid evolutionary divergence. To date, most recent empirical studies of antagonistic coevolution have emphasized only a few taxa. This study uses the abundant but little-used data in the taxonomic literature on morphology to evaluate the roles of antagonistic coevolution and traditional female choice over a wide taxonomic spectrum (61 families of arthropods, mostly insects and spiders). Groups with species-specific male structures that contact females were checked for coevolution of species-specific female structures that are contacted by the male and that have mechanical properties that could potentially defend her against the male. Facultatively deployable, species-specific female defensive structures, a design that would seem likely to evolve frequently under the sexually antagonistic coevolution hypothesis, were completely absent (0% of 106 structures in 84 taxonomic groups). Although likely cases of sexually antagonistic coevolution exist, using conservative criteria, 79.2% of the 106 structures lacked even potentially defensive female coevolution. A common pattern (53.8% of 106) was a nearly complete absence of female change in areas contacted by species-specific male structures. Post-hoc arguments invoking possible coevolution of defensive female behavior instead of morphology, or of female sensitivities and responses to male sensory traps, could enable the sexually antagonistic coevolution hypothesis to explain these data. No case of such coevolution of female behavior or sensitivities has been demonstrated, and there are additional reasons to doubt that they are general explanations for the data presented here. Detailed studies of female resistance behavior could help illuminate several issues. The possibility of a greater role for antagonistic coevolution in reproductive physiology than in morphology and the possibility that female choice and sexually antagonistic coevolution have both been important in some lineages are discussed.     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

Sexual selection on bushcricket genitalia operates in a mosaic pattern

In most species with internal fertilization, male genitalia evolve faster than other morphological structures. This holds true for genital titillators, which are used exclusively during mating in several bushcricket subfamilies. Several theories have been proposed for the sexual selection forces driving the evolution of internal genitalia, especially sperm competition, sexually antagonistic coevolution (SAC), and cryptic female choice (CFC). However, it is unclear whether the evolution of genitalia can be described with a single hypothesis or a combination of them. The study of species‐specific genitalia action could contribute to the controversial debate about the underlying selective evolutionary forces. We studied female mating behaviors in response to experimentally modified titillators in a phylogenetically nested set of four bushcricket species: Roeseliana roeselii, Pholidoptera littoralis littoralis, Tettigonia viridissima (of the subfamily Tettigoniinae), and Letana inflata (Phaneropterinae). Bushcricket titillators have several potential functions; they stimulate females and suppress female resistance, ensure proper ampulla or spermatophore attachment, and facilitate male fixation. In R. roeselii, titillators stimulate females to accept copulations, supporting sexual selection by CFC. Conversely, titillator modification had no observable effect on the female's behavior in T. viridissima. The titillators of Ph. l. littoralis mechanically support the mating position and the spermatophore transfer, pointing to sexual selection by SAC. Mixed support was found in L. inflata, where manipulation resulted in increased female resistance (evidence for CFC) and mating failures by reduced spermatophore transfer success (evidence for SAC). Sexual selection is highly species‐specific with a mosaic support for either cryptic female choice or sexually antagonistic coevolution or a combination of both in the four species.     

Cryptic female exaggeration: the asymmetric female internal genitalia of Kaliana yuruani (Araneae: Pholcidae)

Males of the Venezuelan pholcid spider Kaliana yuruani have unique genitalia, with the procursi about six times as long as usual in the family. The present article describes the previously unknown female, searching for a morphological correlate in the female genitalia to the male's exaggeration. Reconstruction of histological serial sections reveals an internal female complexity that is unequalled in pholcid spiders. An intricate system of ducts and folds is arranged in an asymmetric way, making this the third known case of genital asymmetry in spiders. The term "cryptic female exaggeration" is used in analogy to cryptic female choice, pointing to the fact that from the outside, the female genitalia do not appear unusual. I propose that cryptic female exaggeration may be relatively common in copulatory structures if male exaggerations need to be evaluated according to the female choice by mechanical fit model. Finally, the evolution of genital asymmetry in spiders is contrasted with that in insects.     

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 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.     

Interaction Between Sexually Antagonistic Selection and Mate Choice in the Evolution of Female Responses to Male Traits

Theoretical analyses of selection on mutations affecting female responsiveness to male traits suggested that sexually antagonistic selection and traditional female choice are not exclusive alternatives. They can act simultaneously on the same female traits, and can either reinforce or act against each other. These analyses do not yield theoretical predictions regarding the relative frequency and importance of the two types of selection on female responsiveness, as the balance between them is affected by complex factors, including the frequency distribution of male traits, and the mechanisms of male action. Male–female interactions differ from many other evolutionary interactions involving potential evolutionary conflict, in that male and female genomes are irretrievably mixed in their offspring, thus increasing the possibility of indirect payoffs to one participant from the traits of its partner.     

The evolution of animal genitalia: distinguishing between hypotheses by single species studies

Rapid evolution of genitalia is one of the most general patterns of morphological diversification in animals. Despite its generality, the causes of this evolutionary trend remain obscure. Several alternative hypotheses have been suggested to account for the evolution of genitalia (notably the lock-and-key, pleiotropism, and sexual selection hypotheses). Here, I argue that thorough intraspecific studies are the key to gaining insight into the patterns and processes of genitalic evolution. Critical assumptions and predictions that may be used to distinguish between the different hypotheses are identified and discussed. However, current knowledge of selection on genitalia, or even of the degree of phenotypic and genotypic variability of genital morphology, is highly limited, allowing only a very tentative assessment of the various hypotheses. In-depth single species studies of current patterns and processes of selection on genitalia are badly needed, and a single species research program is briefly outlined.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

The evolution of female genitalia

Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long‐standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison with male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here, we examine evidence for three mechanisms of genital evolution in females: species isolating ‘lock‐and‐key’ evolution, cryptic female choice and sexual conflict. Lock‐and‐key genital evolution has been thought to be relatively unimportant; however, we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species; however, the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution.     

Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera)

Sperm morphometry is extremely variable across species, but a general adaptive explanation for this diversity is lacking. As sperm must function within the female, variation in sperm form may be associated with variation in female reproductive tract morphology. We investigated this and other potential evolutionary associations between male and female reproductive characters across the Scathophagidae. Sperm length was positively associated with the length of the spermathecal (sperm store) ducts, indicating correlated evolution between the two. No association was found between sperm length and spermathecal size. However, the size of the spermathecae was positively associated with testis size indicating co-evolution between male investment in sperm production and female sperm storage capacity. Furthermore, species with a higher degree of polyandry (larger testes) had longer spermathecal ducts. However, no associations between sperm length or length variation and testis size were found which suggests greater sperm competition sensu stricto does not select for longer sperm.     

Postmating sexual selection: allopatric evolution of sperm competition mechanisms and genital morphology in calopterygid damselflies (Insecta: Odonata)

Postmating sexual selection theory predicts that in allopatry reproductive traits diverge rapidly and that the resulting differentiation in these traits may lead to restrictions to gene flow between populations and, eventually, reproductive isolation. In this paper we explore the potential for this premise in a group of damselflies of the family Calopterygidae, in which postmating sexual mechanisms are especially well understood. Particularly, we tested if in allopatric populations the sperm competition mechanisms and genitalic traits involved in these mechanisms have indeed diverged as sexual selection theory predicts. We did so in two different steps. First, we compared the sperm competition mechanisms of two allopatric populations of Calopteryx haemorrhoidalis (one Italian population studied here and one Spanish population previously studied). Our results indicate that in both populations males are able to displace spermathecal sperm, but the mechanism used for sperm removal between both populations is strikingly different. In the Spanish population males seem to empty the spermathecae by stimulating females, whereas in the Italian population males physically remove sperm from the spermathecae. Both populations also exhibit differences in genital morphometry that explain the use of different mechanisms: the male lateral processes are narrower than the spermathecal ducts in the Italian population, which is the reverse in the Spanish population. The estimated degree of phenotypic differentiation between these populations based on the genitalic traits involved in sperm removal was much greater than the differentiation based on a set of other seven morphological variables, suggesting that strong directional postmating sexual selection is indeed the main evolutionary force behind the reproductive differentiation between the studied populations. In a second step, we examined if a similar pattern in genital morphometry emerge in allopatric populations of this and other three species of the same family (Calopteryx splendens, C. virgo and Hetaerina cruentata). Our results suggest that there is geographic variation in the sperm competition mechanisms in all four studied species. Furthermore, genitalic morphology was significantly divergent between populations within species even when different populations were using the same copulatory mechanism. These results can be explained by probable local coadaptation processes that have given rise to an ability or inability to reach and displace spermathecal sperm in different populations. This set of results provides the first direct evidence of intraspecific evolution of genitalic traits shaped by postmating sexual selection.     

Rapid evolution of pollen and pistil traits as a response to sexual selection in the post-pollination phase of mating

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One size fits all? Determinants of sperm transfer in a highly dimorphic orb‐web spider

The evolutionary significance of widespread hypo‐allometric scaling of genital traits in combination with rapid interspecific genital trait divergence has been of key interest to evolutionary biologists for many years and remains poorly understood. Here, we provide a detailed assessment of quantitative genital trait variation in males and females of the sexually highly dimorphic and cannibalistic orb‐weaving spider Argiope aurantia. We then test how this trait variation relates to sperm transfer success. In particular, we test specific predictions of the one‐size‐fits‐all and lock‐and‐key hypotheses for the evolution of genital characters. We use video‐taped staged matings in a controlled environment with subsequent morphological microdissections and sperm count analyses. We find little support for the prediction of the one‐size‐fits‐all hypothesis for the evolution of hypo‐allometric scaling of genital traits, namely that intermediate trait dimensions confer highest sperm transfer success. Likewise, our findings do not support the prediction of the lock‐and‐key hypothesis that a tight fit of male and female genital traits mediates highest sperm transfer success. We do, however, detect directional effects of a number of male and female genital characters on sperm transfer, suggesting that genital trait dimensions are commonly under selection in nature. Importantly, even though females are much larger than males, spermatheca size limits the number of sperm transferred, contradicting a previous hypothesis about the evolutionary consequences of genital size dimorphism in extremely size‐dimorphic taxa. We also find strong positive effects of male body size and copulation duration on the probability of sperm transfer and the number of sperm transferred, with implications for the evolution of extreme sexual size dimorphism and sexual cannibalism in orb weavers.     

The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders

Under natural and sexual selection traits often evolve that secure paternity or maternity through self‐sacrifice to predators, rivals, offspring, or partners. Emasculation—males removing their genitals—is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm‐transferring organs — secondary genitals — (hereafter, palps), results in ‘eunuchs’. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male–male contests (better‐fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves‐off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote‐copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb‐weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: ‘pre‐maturation’, ‘mating’, and ‘post‐mating’. We use a genus‐level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co‐evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.