Increased copulation duration before ejaculate transfer is associated with larger spermatophores, and male genital titillators, across bushcricket taxa

Copulation duration varies considerably across species, but few comparative studies have examined factors that might underlie such variation. We examined the relationship between copulation duration (prior to spermatophore transfer), the complexity of titillators (sclerotized male genital contact structures), spermatophore mass and male body mass across 54 species of bushcricket. Using phylogenetic comparative analyses, we found that copulation duration was much longer in species with titillators than those without, but it was not longer in species with complex compared with simple titillators. A positive relationship was found between spermatophore size and copulation duration prior to ejaculate transfer, which supports the hypothesis that this represents a period of mate assessment. The slope of this relationship was steeper in species with simple rather than complex titillators. Although the data suggest that the presence of titillators is necessary to maintain long copulation prior to ejaculate transfer, mechanisms underlying this association remain unclear.     

Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia

Sexual conflict over mating can result in sex-specific morphologies and behaviours that allow each sex to exert control over the outcome of reproduction. Genital traits, in particular, are often directly involved in conflict interactions. Via genital manipulation, we experimentally investigated whether genital traits in red-sided garter snakes influence copulation duration and formation of a copulatory plug. The hemipenes of male red-sided garter snakes have a large basal spine that inserts into the female cloaca during mating. We ablated the spine and found that males were still capable of copulation but copulation duration was much shorter and copulatory plugs were smaller than those produced by intact males. We also anaesthetized the female cloacal region and found that anaesthetized females copulated longer than control females, suggesting that female cloacal and vaginal contractions play a role in controlling copulation duration. Both results, combined with known aspects of the breeding biology of red-sided garter snakes, strongly support the idea that sexual conflict is involved in mating interactions in this species. Our results demonstrate the complex interactions among male and female traits generated by coevolutionary processes in a wild population. Such complexity highlights the importance of simultaneous examination of male and female traits.     

Intra-specific variation in the morphology and the benefit of large genital sclerites of males in the adzuki bean beetle (Callosobruchus chinensis)

Rapid evolution has led to a large diversity in the sizes and morphology of male genitals across taxa, but the mechanisms driving this evolution remain controversial. In this study, we investigated the function of male genital sclerites in the adzuki bean beetle (Callosobruchus chinensis) and compared the length and morphology of genital sclerites between two populations that vary in their degree of polyandry. We found that the length of male genital sclerites was negatively correlated with copulation duration but positively correlated with the speed of matings with multiple females. Additionally, we found that the average length and number of genital sclerite spines of males from the more polyandrous population were larger than those from the less polyandrous population. We suggest that the genital sclerite of male adzuki bean beetles evolved by sexual selection, and a larger genital sclerite has a selective advantage because it allows for rapid copulations with multiple females.     

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

Hypotheses regarding the function of elaborate male genitalia were tested in a sample of insects and spiders by comparing their allometric values (slopes in log-log regressions on indicators of body size) with those of other body parts. Male genitalia consistently had lower slopes than other body parts. Perhaps as a consequence of this pattern, genitalic size also tended, though less consistently, to have lower coefficients of variation than did the size of other body parts. The morphological details of coupling between males and females in several species clearly indicated that selection favoring mechanical fit is not responsible for these trends. Sexual selection on male courtship structures that are brought into contact with females in precise ways may favor relatively low allometric values, in contrast to the high values seen in the other sexually selected characters (usually visual display devices) that have been studied previously, because a female's own size will influence her perception of the contact courtship devices of a male.     

Male mating success and survival in the field with respect to size and courtship song characters inDrosophila littoralis andD. montana (Diptera: Drosophilidae)

We investigated the importance of male song and morphological characters to the male mating success in a two-year field study in natural populations ofD. littoralis andD. montana. We compared the properties of mating flies with those of a random male sample taken at the same time and place. InD. littoralis the male's size had no effect on his mating success, while inD. montana small males had a mating advantage in the field during the first study year. Females preferred males with short sound pulses in both species. We also examined the relationship between male morphological and song characters and viability by collecting male flies in late summer and comparing the means of male characters to those of overwintered flies the next spring. InD. littoralis male size had no effect on overwinter survival. InD. montana large flies survived better than small flies. In both species the shifts in song characters during the winter dormancy were opposite to those caused by sexual selection. Our results, accordingly, imply a possible balance between the forces of sexual and natural selection, which act in opposing directions on attractive male traits.     

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the ‘one‐size‐fits‐all’ hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One‐size‐fits‐all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One‐size‐fits‐all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.     

Precisely proportioned: intertidal barnacles alter penis form to suit coastal wave action

For their size, barnacles possess the longest penis of any animal (up to eight times their body length). However, as one of few sessile animals to copulate, they face a trade-off between reaching more mates and controlling ever-longer penises in turbulent flow. We observed that penises of an intertidal barnacle (Balanus glandula) from wave-exposed shores were shorter than, stouter than, and more than twice as massive for their length as, those from nearby protected bays. In addition, penis shape variation was tightly correlated with maximum velocity of breaking waves, and, on all shores, larger barnacles had disproportionately stouter penises. Finally, field experiments confirmed that most of this variation was due to phenotypic plasticity: barnacles transplanted to a wave-exposed outer coast produced dramatically shorter and wider penises than counterparts moved to a protected harbour. Owing to the probable trade-off between penis length and ability to function in flow, and owing to the ever-changing wave conditions on rocky shores, intertidal barnacles appear to have acquired the capacity to change the size and shape of their penises to suit local hydrodynamic conditions. This dramatic plasticity in genital form is a valuable reminder that factors other than the usual drivers of genital diversification--female choice, sexual conflict and male-male competition--can influence genital form.     

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

Male genitalia in Drosophila exemplify strikingly rapid and divergent evolution, whereas female genitalia are relatively invariable. Whereas precopulatory and post-copulatory sexual selection has been invoked to explain this trend, the functional significance of genital structures during copulation remains obscure. We used time-sequence analysis to study the functional significance of external genitalic structures during the course of copulation, between D. melanogaster and D. simulans. This functional analysis has provided new information that reveals the importance of male-driven copulatory mechanics and strategies in the rapid diversification of genitalia. The posterior process, which is a recently evolved sexual character and present only in males of the melanogaster clade, plays a crucial role in mounting as well as in genital coupling. Whereas there is ample evidence for precopulatory and/or post-copulatory female choice, we show here that during copulation there is little or no physical female choice, consequently, males determine copulation duration. We also found subtle differences in copulatory mechanics between very closely related species. We propose that variation in male usage of novel genitalic structures and shifts in copulatory behaviour have played an important role in the diversification of genitalia in species of the Drosophila subgroup.