Postcopulatory Sexual Selection Research Articles

Multivariate selection drives concordant patterns of pre- and postcopulatory sexual selection in a livebearing fish.

In many species, females mate with multiple partners, meaning that sexual selection on male traits operates across a spectrum that encompasses the competition for mates (that is, before mating) and fertilizations (after mating). Despite being inextricably linked, pre- and postcopulatory sexual selection are typically studied independently, and we know almost nothing about how sexual selection operates across this divide. Here we bridge this knowledge gap using the livebearing fish Poecilia reticulata. We show that both selective episodes, as well as their covariance, explain a significant component of variance in male reproductive fitness. Moreover, linear and nonlinear selection simultaneously act on pre- and postcopulatory traits, and interact to generate multiple phenotypes with similar fitness.

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter-male variation (CVbm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra-pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage-specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.

Vibrational Signals and Mating Behavior of Japanese Beetles (Coleoptera: Scarabaeidae)

ABSTRACT We report that male Japanese beetles produce substrate-borne vibrational signals during mating. Males produced these signals while mounted on the female, mainly before genital intromission but also during intromission and afterwards during mate guarding. Females thus likely perceive male signals as contact courtship. We also describe new details of male mating behavior, including stroking the female with the forelegs.We discuss the likely function of male signaling and stroking behavior as courtship in the context of pre- and postcopulatory sexual selection.

Function of copulatory plugs in house mice: mating behavior and paternity outcomes of rival males

Polyandry is widespread across animal taxa, and subjects males to intense post-copulatory sexual selection which favors adaptations that enhance a male’s paternity success, either by decreasing the risk of sperm competition and/or by increasing the competitiveness of the ejaculate. Copulatory plugs deposited by males are thought to have evolved in the context of sperm competition. However, experimental studies that assess the function of copulatory plugs remain scarce. Moreover, most studies have used unnatural manipulations, such as ablating plug-producing male glands or interrupting copulations. Here, we investigated whether repeated ejaculation affects plug size in a mammalian model species, the house mouse. When males experience short periods of sexual rest we found that plug size decreased over repeated ejaculations so that time since last ejaculation can be applied as an approximation for plug size. We induced natural variation in plug size arising from variation in male sexual restedness, and investigated the behavior and paternity success of rival males. Male behavior in the offensive mating role (second) was influenced, albeit not significantly, by the sexual restedness of the first male-to-mate, and therefore the size of his plug. However, second males sired a significantly greater proportion of embryos when competing against a male that had recently mated compared to a male that had not. This supports a potential role of the plug in promoting a male's competitive fertilization success when remating occurs, which could be mediated both by delaying female remating and by ensuring efficient sperm transport through the female reproductive tract.

No evidence of trade-offs in the evolution of sperm numbers and sperm size in mammals.

Post-copulatory sexual selection, in the form sperm competition, has influenced the evolution of several male reproductive traits. However, theory predicts that sperm competition would lead to trade-offs between numbers and size of spermatozoa because increased costs per cell would result in a reduction of sperm number if both traits share the same energetic budget. Theoretical models have proposed that, in large animals, increased sperm size would have minimal fitness advantage compared with increased sperm numbers. Thus, sperm numbers would evolve more rapidly than sperm size under sperm competition pressure. We tested in mammals whether sperm competition maximizes sperm numbers and size, and whether there is a trade-off between these traits. Our results showed that sperm competition maximizes sperm numbers in eutherian and metatherian mammals. There was no evidence of a trade-off between sperm numbers and sperm size in any of the two mammalian clades as we did not observe any significant relationship between sperm numbers and sperm size once the effect of sperm competition was taken into account. Maximization of both numbers and size in mammals may occur because each trait is crucial at different stages in sperm's life; for example size-determined sperm velocity is a key determinant of fertilization success. In addition, numbers and size may also be influenced by diverse energetic budgets required at different stages of sperm formation.

High opportunity for postcopulatory sexual selection under field conditions.

In polygamous systems, male fitness is determined not only by mating success but also by fertilization success. Despite the growing interest over the past several decades in postcopulatory sexual selection, its relative importance compared to precopulatory sexual selection remains a subject of debate. Here, we use extensive behavioral observations of a seminatural population of Hawaiian swordtail crickets, Laupala cerasina, and molecular paternity assignment to measure the opportunities for pre- and postcopulatory selection. Because postcopulatory selection has the potential to operate at multiple stages, we also separately attribute its effects to factors specific to mating events versus factors specific to males. We find that variance in postcopulatory success is over four times as great as variance in precopulatory success, with most of it unexplained by male mating order or the number of nuptial gifts given. Surprisingly, we also find that male singing effort is under postcopulatory selection, suggesting that males who sing more frequently also have more competitive ejaculates. Our results are consistent with the hypothesis that high polyandry levels promote greater relative postcopulatory selection. They also highlight the need for detailed behavioral observations under conditions as natural as possible when measuring mating and reproductive success.

A trade-off between pre- and post-copulatory sexual selection in a bean beetle

It is now generally recognized that it is necessary to examine how sexual selection operates across the lifespan of a male, in order to understand the total sexual selection in action. However, less attention has been paid to the fact that selection pressures can change in response to varying environmental conditions. Here, we examine male allocation to trait subject to pre- and post-copulatory sexual selection in Callosobruchus chinensis. We find evidence of a trade-off between dispersal ability and testes size and sperm transfer, across geographical strains. In addition, male mating success of strains with larger testes and better dispersal ability, respectively, changed in response to environmental conditions. Males with better dispersal ability had greater success in securing mates, compared to males with larger testes, under conditions where it was harder to find females. There was no difference in male ability to secure mates when it was easy for them to find females. However, we suggest that males with larger testes are likely to have an advantage in sperm competition under conditions where it is easier to find females, and when females are thus likely to mate multiply. Our results indicate that environmental fluctuations and trade-offs can work in conjunction to maintain alternative male behavioral reproductive strategies.

Sexual rest and post-meiotic sperm ageing in house mice.

Fertilization by aged sperm can result in adverse fitness consequences for both males and females. Sperm storage during male sexual rest could provide an environment for post-meiotic sperm senescence causing a deterioration in the quality of stored sperm, possibly impacting on both sperm performance (e.g. swimming ability) and DNA quality. Here, we compared the proportion of sperm with fragmented DNA, an indicator of structural damage of DNA within the sperm cell, among males that had been sexually rested for approximately 2 months, to that of males that had mated recently. We found no evidence of intra-epididymal sperm DNA damage or any impairment in sperm performance, and consequently no evidence of post-meiotic sperm senescence. Our results suggest that male house mice are likely to possess mechanisms that function to ensure that their sperm reserves remain stocked with 'young', viable sperm during periods of sexual inactivity. We also discuss the possibility that our experimental design leads to no difference in the age of sperm among males from the two mating treatments. Post-meiotic sperm senescence is especially relevant under sperm competition. Thus, we sourced mice from populations that differed in their levels of post-copulatory sexual selection, enabling us to gain insight into how selection for higher sperm production influences the rate of sperm ageing and levels of DNA fragmentation. We found that males from the population that produced the highest number of sperm also had the smallest proportion of DNA-fragmented sperm and discuss this outcome in relation to selection acting upon males to ensure that they produce ejaculates with high-quality sperm that are successful in achieving fertilizations under competitive conditions.

Postcopulatory sexual selection favors fertilization success of restocking hybrid quails over native Common quails (Coturnix coturnix)

Postcopulatory sexual selection plays an important role in the reproductive success of males in many species. Differences in fertilization success could affect rates of admixture and genetic introgression between divergent lineages. We investigated sperm precedence in matings in captivity involving Common quails (Coturnix coturnix) and farm quails of hybrid origin (C. coturnix × domestic Japanese quail, C. japonica), the last used in restocking practices to increase hunting bags. These inter-specific matings in natural conditions are claimed to represent an important threat to the conservation of native Common quail populations. Results showed that fertilization success of each male depended on (1) the time it spent with the female, (2) the presence of sperm from a previous male in the female oviduct, (3) the time that the previous partner had been copulating with the female, and, most importantly, (4) the genetic origin of the male (wild or farm). Farm hybrid males showed higher fertilization success than wild Common males, and they required less time with the female to fertilize the same proportion of eggs. The presence of sperm from another male in the female oviduct reduced the percentage of fertilized eggs by a male. However, this reduction was higher for wild males when the precedent mate was a farm male. In summary, the sperm of farm hybrid males may outcompete the sperm of native males and this could be favoring the introgression of domestic Japanese alleles into the Common quail population, thus constituting a severe conservation threat to wild Common quail populations.

The Gerbil Spermatozoon – interspecific variation in morphology does not invariably follow murine rodent evolutionary trends in response to predicted intermale sperm competition

AbstractIn various groups of mammals, the intensity of intermale sperm competition relates to relative testes mass (RTM) with some evidence suggesting that this may also be the case for some aspects of sperm form. In murid rodents, a large RTM generally correlates with a streamlined sperm head, long apical hook and long tail with most data coming from species in the subfamily Murinae. In this study, RTM and sperm form are compared across 15 species of gerbils, seven from the Tribe Taterillini and eight from the Tribe Gerbillini. Marked interspecific differences in RTM and sperm morphology were observed. However, the Gerbilliscus species with the largest RTM do not have a sperm head with an apical hook nor a longer sperm tail than other species with smaller RTM whereas, by contrast, in the Tribe Gerbillini, species where the sperm head lacks a hook have a relatively small testes mass. We thus suggest that in gerbils, unlike in murine rodents, high levels of postcopulatory sexual selection have not invariably resulted in the evolution of a spermatozoon with a long apical hook and long sperm tail. The possible reasons for this are briefly discussed.

The effects of food limitation on life history tradeoffs in pregnant male gulf pipefish.

Syngnathid fishes (pipefishes, seahorses and seadragons) are characterized by a unique mode of paternal care in which embryos develop on or in the male’s body, often within a structure known as a brood pouch. Evidence suggests that this pouch plays a role in mediating postcopulatory sexual selection and that males have some control over the events occurring within the pouch during the pregnancy. These observations lead to the prediction that males should invest differently in broods depending on the availability of food. Here, we use the Gulf pipefish to test this prediction by monitoring growth rate and offspring survivorship during the pregnancies of males under low- or high-food conditions. Our results show that pregnant males grow less rapidly on average than non-pregnant males, and pregnant males under low-food conditions grow less than pregnant males under high-food conditions. Offspring survivorship, on the other hand, does not differ between food treatments, suggesting that male Gulf pipefish sacrifice investment in somatic growth, and thus indirectly sacrifice future reproduction, in favor of current reproduction. However, a positive relationship between number of failed eggs and male growth rate in our low-food treatments suggests that undeveloped eggs reduce the pregnancy’s overall cost to the male compared to broods containing only viable offspring.

How did viviparity originate and evolve? Of conflict, co-option, and cryptic choice.

I propose that the underlying adaptation enabling the reproductive strategy of birthing live young (viviparity) is retraction of the site of fertilization within the female reproductive tract, and that this evolved as a means of postcopulatory sexual selection. There are three conspicuous aspects associated with viviparity: (i) internal development is a complex trait often accompanied by a suite of secondary adaptations, yet it is unclear how the intermediate state of this trait - egg retention - could have evolved; (ii) viviparity often results in a reduction in fecundity; (iii) viviparity has evolved independently many times across a diverse array of animal groups. Focusing on the Diptera (true flies), I provide explanations for these observations. I further propose that fecundity is not traded-off to enable potential benefits of viviparity, but rather that loss of fecundity is directly selected and egg retention is an indirect consequence - a model that provides a unifying common basis for the ubiquity of viviparity.

Contrasting life history and reproductive traits in two populations of Scyliorhinus canicula

The role of natural and sexual selection in generating variability in biological traits between populations represents an intriguing issue in evolutionary biology. Considering their occurrence in different environments and the extensive incidence of post-copulatory sexual selection, elasmobranchs represent an interesting, yet still poorly investigated group. In this study, the life history and reproductive traits of two populations of Scyliorhinus canicula from the northern Adriatic Sea and the Strait of Sicily were compared. Differences in maximum size and size at sexual maturity were observed. The two populations also displayed differences in male and female genitalia. Males in the northern Adriatic Sea presented heavier testes, longer epididymis, seminal vesicles and claspers compared with those in the Strait of Sicily, suggesting the occurrence of stronger sperm competition at the former site. Similarly, females in the northern Adriatic Sea showed heavier oviducal glands and longer reproductive tracts compared with those in the Strait of Sicily. The coevolution between male and female genitalia suggests the occurrence of stronger sexual conflict and/or cryptic female choice in the population from the northern Adriatic Sea. Therefore, natural selection, represented by the different selective pressures occurring at different latitudes, and sexual selection, represented by potentially differing strengths of post-copulatory sexual selection and sexual conflict, may act individually in driving divergence in life history and reproductive traits in these two populations of S. canicula.

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology.

Rapid diversification of sexual traits is frequently attributed to sexual selection, though explicit tests of this hypothesis remain limited. Spermatozoa exhibit remarkable variability in size and shape, and studies report a correlation between sperm morphology (sperm length and shape) and sperm competition risk or female reproductive tract morphology. However, whether postcopulatory processes (e.g., sperm competition and cryptic female choice) influence the speed of evolutionary diversification in sperm form is unknown. Using passerine birds, we quantified evolutionary rates of sperm length divergence among lineages (i.e., species pairs) and determined whether these rates varied with the level of sperm competition (estimated as relative testes mass). We found that relative testes mass was significantly and positively associated with more rapid phenotypic divergence in sperm midpiece and flagellum lengths, as well as total sperm length. In contrast, there was no association between relative testes mass and rates of evolutionary divergence in sperm head size, and models suggested that head length is evolutionarily constrained. Our results are the first to show an association between the strength of sperm competition and the speed of sperm evolution, and suggest that postcopulatory sexual selection promotes rapid evolutionary diversification of sperm morphology.

Evolutionary change in testes tissue composition among experimental populations of house mice.

Theory assumes that postcopulatory sexual selection favors increased investment in testes size because greater numbers of sperm within the ejaculate increase the chance of success in sperm competition, and larger testes are able to produce more sperm. However, changes in the organization of the testes tissue may also affect sperm production rates. Indeed, recent comparative analyses suggest that sperm competition selects for greater proportions of sperm-producing tissue within the testes. Here, we explicitly test this hypothesis using the powerful technique of experimental evolution. We allowed house mice (Mus domesticus) to evolve via monogamy or polygamy in six replicate populations across 24 generations. We then used histology and image analysis to quantify the proportion of sperm-producing tissue (seminiferous tubules) within the testes of males. Our results show that males that had evolved with sperm competition had testes with a higher proportion of seminiferous tubules compared with males that had evolved under monogamy. Previously, it had been shown that males from the polygamous populations produced greater numbers of sperm in the absence of changes in testes size. We thus provide evidence that sperm competition selects for an increase in the density of sperm-producing tissue, and consequently increased testicular efficiency.

A Neuronal Pathway that Controls Sperm Ejection and Storage in Female Drosophila

In polyandrous females, sperm storage permits competition between sperm of different mates, and in some species females influence the relative fertilization success of competing sperm in favor of a preferred mate [1, 2]. In female Drosophila melanogaster, sperm competition is strongly influenced by the timing of sperm ejection from the uterus [3, 4]. Understanding how female behavior influences sperm competition requires knowledge of the neuronal mechanisms controlling sperm retention and storage, which is currently lacking. Here, we show that D.melanogaster females eject male ejaculates from the uterus 1-6hr after mating with a stereotypic behavior regulated by a brain signaling pathway composed of diuretic hormone 44 (Dh44), a neuropeptide related to vertebrate corticotropin-releasing factor (CRF), and its receptor, Dh44R1. Suppression of Dh44 signals in the brain expedites sperm ejection from the uterus, resulting in marked reduction of sperm in the storage organs and decreased fecundity, whereas enhancement of Dh44 signals delays sperm expulsion. The Dh44 function was mapped to six neurons located in the pars intercerebralis of the brain together with a small subset of Dh44R1 neurons that express the sex-specific transcription factor doublesex. This study identifies a neuronal pathway by which females can control sperm retention and storage and provides new insight into how the female might exercise post-copulatory sexual selection.

Intra‐ and intermale variability of mature sperm traits analysed in two brackish water populations of the pipefish Syngnathus abaster (Syngnathidae)

AbstractSperm cells are highly diversified in animals, and considerable research effort has focused on variation in sperm morphology among species. Surprisingly, little is known about intraspecific variation in sperm morphology. We analysed within‐ and between‐male variation in mature sperm traits in two brackish water populations of the pipefish Syngnathus abaster. Four morphometric parameters, such as the width and length of the head (including nucleus, and midpiece), length of flagellum and total sperm length were taken into account. The differences in all morphometric parameters analysed between populations were not statistically significant. Moreover, the multidimensional scaling analysis shows that (i) the two populations seem to be indistinguishable based on their spermatozoa and (ii) there is not polymorphism, being sperm not distinguishable into discrete classes both within a single male and between males of each populations. The latter datum does not seem to support the presence of polymorphic sperm in syngnathids. Both populations, however, exhibit a high variation in all sperm traits, both among individual sperm within an ejaculate and among males within each population. The relationship between sperm traits variability and the low selection pressure determined by the absence of postcopulatory sexual selection (i.e. absence of sperm competition) is discussed.

Diet affects ejaculate traits in a lizard with condition-dependent fertilization success

Sexually selected traits are often driven to costly extremes by persistent directional selection. Energy acquisition and allocation can therefore influence variation in traits subject to both precopulatory and postcopulatory sexual selection, though the later have received much less attention. We tested the condition dependence of sperm morphology, sperm count, and fertilization success in a promiscuous lizard (Anolis sagrei) by 1) collecting sperm samples from wild males that varied naturally in body condition, 2) experimentally altering the body condition of captive males through dietary restriction, and 3) analyzing genetic paternity data from competitive mating trials between captive males that differed in body condition. In both wild and captive males, the length of the sperm midpiece decreased with body condition. Experimental food restriction decreased sperm production, decreased length of the sperm head, increased length of the sperm midpiece, and increased variance in sperm morphology within individuals. When restricted to a single copulation, males on high-intake diets exhibited a slight but nonsignificant fertilization advantage. Reanalysis of a previous experiment in which high- and low-condition males were sequentially allowed to copulate ad libitum for 1 week revealed a significant fertilization bias in favor of high-condition males. When controlling for mean treatment effects on the proportion of offspring sired and on sperm phenotypes, multiple regression revealed negative correlations between fertilization success and sperm head length, midpiece length, and sperm count. Collectively, our results suggest that condition-dependent fertilization success in A. sagrei may be partially mediated by underlying condition dependence of sperm morphology and sperm count.

Characterizing male-female interactions using natural genetic variation in Drosophila melanogaster.

Drosophila melanogaster females commonly mate with multiple males establishing the opportunity for pre- and postcopulatory sexual selection. Traits impacting sexual selection can be affected by a complex interplay of the genotypes of the competing males, the genotype of the female, and compatibilities between the males and females. We scored males from 96 2nd and 94 3rd chromosome substitution lines for traits affecting reproductive success when mated with females from 3 different genetic backgrounds. The traits included male-induced female refractoriness, male remating ability, the proportion of offspring sired under competitive conditions and male-induced female fecundity. We observed significant effects of male line, female genetic background, and strong male by female interactions. Some males appeared to be "generalists" and performed consistently across the different females; other males appeared to be "specialists" and performed very well with a particular female and poorly with others. "Specialist" males did not, however, prefer to court those females with whom they had the highest reproductive fitness. Using 143 polymorphisms in male reproductive genes, we mapped several genes that had consistent effects across the different females including a derived, high fitness allele in Acp26Aa that may be the target of adaptive evolution. We also identified a polymorphism upstream of PebII that may interact with the female genetic background to affect male-induced refractoriness to remating. These results suggest that natural variation in PebII might contribute to the observed male-female interactions.

Evaluating the post-copulatory sexual selection hypothesis for genital evolution reveals evidence for pleiotropic harm exerted by the male genital spines of Drosophila ananassae.

The contemporary explanation for the rapid evolutionary diversification of animal genitalia is that such traits evolve by post-copulatory sexual selection. Here, we test the hypothesis that the male genital spines of Drosophila ananassae play an adaptive role in post-copulatory sexual selection. Whereas previous work on two Drosophila species shows that these spines function in precopulatory sexual selection to initiate genital coupling and promote male competitive copulation success, further research is needed to evaluate the potential for Drosophila genital spines to have a post-copulatory function. Using a precision micron-scale laser surgery technique, we test the effect of spine length reduction on copulation duration, male competitive fertilization success, female fecundity and female remating behaviour. We find no evidence that male genital spines in this species have a post-copulatory adaptive function. Instead, females mated to males with surgically reduced/blunted genital spines exhibited comparatively greater short-term fecundity relative to those mated by control males, indicating that the natural (i.e. unaltered) form of the trait may be harmful to females. In the absence of an effect of genital spine reduction on measured components of post-copulatory fitness, the harm seems to be a pleiotropic side effect rather than adaptive. Results are discussed in the context of sexual conflict mediating the evolution of male genital spines in this species and likely other Drosophila.