Postcopulatory Sexual Selection Research Articles

Matrotrophy and polyandry partially regulate postcopulatory mechanisms and sexual selection in a bimodal viviparous salamander

Matrotrophy and polyandry partially regulate postcopulatory mechanisms and sexual selection in a bimodal viviparous salamander

Male allocation to ejaculation and mating effort imposes different life history trade-offs.

When males compete, sexual selection favors reproductive traits that increase their mating or fertilization success (pre- and postcopulatory sexual selection). It is assumed that males face a trade-off between these 2 types of sexual traits because they both draw from the same pool of resources. Consequently, allocation into mate acquisition or ejaculation should create similar trade-offs with other key life history traits. Tests of these assumptions are exceedingly rare. Males only ejaculate after they mate, and the costs of ejaculation are therefore highly confounded with those of mating effort. Consequently, little is known about how each component of reproductive allocation affects a male's future performance. Here, we ran an experiment using a novel technique to distinguish the life history costs of mating effort and ejaculation for mosquitofish (Gambusia holbrooki). We compared manipulated males (mate without ejaculation), control males (mate and ejaculate), and naïve males (neither mate nor ejaculate) continuously housed with a female and 2 rival males. We assessed their growth, somatic maintenance, mating and fighting behavior, and sperm traits after 8 and 16 weeks. Past mating effort significantly lowered a male's future mating effort and growth, but not his sperm production, while past sperm release significantly lowered a male's future ejaculate quantity, but not his mating effort. Immune response was the only trait impacted by both past mating effort and past ejaculation. These findings challenge the assumption that male reproductive allocation draws from a common pool of resources to generate similar life history costs later in life. Instead, we provide clear evidence that allocation into traits under pre- and postcopulatory sexual selection have different trait-specific effects on subsequent male reproductive performance.

Sperm competition favours intermediate sperm size in a hermaphrodite.

Sperm competition is a potent mechanism of post-copulatory sexual selection that has been found to shape reproductive morphologies and behaviours in promiscuous animals. Especially sperm size has been argued to evolve in response to sperm competition through its effect on sperm longevity, sperm motility, the ability to displace competing sperm and ultimately fertilization success. Additionally, sperm size has been observed to co-evolve with female reproductive morphology. Theoretical work predicts that sperm competition may select for longer sperm but may also favour shorter sperm if sperm size trades off with number. In this study, we studied the relationship between sperm size and post-mating success in the free-living flatworm, Macrostomum lignano. Specifically, we used inbred isolines of M. lignano that varied in sperm size to investigate how sperm size translated into the ability of worms to transfer and deposit sperm in a mating partner. Our results revealed a hump-shaped relationship with individuals producing sperm of intermediate size having highest sperm competitiveness. This finding broadens our understanding of the evolution of sperm morphology by providing empirical support for stabilizing selection on sperm size under sperm competition.

Paternity bias and cryptic female choice in chickens

Sperm competition and cryptic female choice (CFC) are two significant mechanisms of postcopulatory sexual selection that greatly impact fertilization success in various species. Despite extensive research has conducted on sperm competition and the evolution of sperm traits in internal fertilizers, our understanding of the female preferences in selecting sperm is still limited. Here, we aimed to investigate the characteristics of CFC in chickens by utilizing artificial insemination with mixed semen to control for variations in male fertilization success caused by female perception of male quality and mating order. Our results revealed that the offspring from multiple-mated females exhibited mixed paternity. Although the males had an equal number of viable sperm, one male consistently exhibited a 15% higher success rate on average, regardless of whether the insemination was performed with fresh or diluted semen. This result suggested that this male demonstrates superior performance in sperm competition, and exhibited a potential advantage in fertilization success. While the dominant male generally made a greater genetic contribution to most offspring, the degree of this advantage varied greatly, ranging from 11.11% to 75.00%. Furthermore, our study provided evidence of female preferences influenced the precedence of sperm from certain males over others. Interestingly, this bias is not consistently observed among all individuals, as offspring derived from some females were predominantly sired by an overall disadvantaged male while others were predominantly by a different disadvantaged male. Overall, these results underscored the complex processes involved in sperm selection and emphasized the importance of females in sexual selection theory.

Sexual Selection Increases Male Behavioral Consistency in Drosophila melanogaster.

AbstractSexual selection has been suggested to influence the expression of male behavioral consistency. However, despite predictions, direct experimental support for this hypothesis has been lacking. Here, we investigated whether sexual selection altered male behavioral consistency in Drosophila melanogaster-a species with both pre- and postcopulatory sexual selection. We took 1,144 measures of locomotor activity (a fitness-related trait in D. melanogaster) from 286 flies derived from replicated populations that have experimentally evolved under either high or low levels of sexual selection for >320 generations. We found that high sexual selection males were more consistent (decreased within-individual variance) in their locomotor activity than male conspecifics from low sexual selection populations. There were no differences in behavioral consistency between females from the high and low sexual selection populations. Furthermore, while females were more behaviorally consistent than males in the low sexual selection populations, there were no sex differences in behavioral consistency in high sexual selection populations. Our results demonstrate that behavioral plasticity is reduced in males from populations exposed to high levels of sexual selection. Disentangling whether these effects represent an evolved response to changes in the intensity of selection or are manifested through nongenetic parental effects represents a challenge for future research.

The evolution of seminal fluid gene expression and postmating reproductive isolation in Drosophila.

Seminal fluid protein (Sfp) genes show, in general, a higher rate of sequence divergence than genes from other categories, which is often attributed to forms of postcopulatory sexual selection or sexual conflict. Recently, the relaxation of selective constraints has been proposed as an alternative explanation for the rapid sequence evolution of Sfps and other genes with sex-limited expression. The expression of Sfp genes is a likely target of selection, but the evolution of differences in their expression levels is less understood. Here, we explore both polymorphism and divergence in Sfp gene expression between Drosophila melanogaster and Drosophila simulans, how selection might have influenced their expression, and whether changes in expression might trigger the evolution of reproductive isolating barriers. In our analysis, Sfp genes showed higher divergence, but not higher polymorphism, in expression than the average male reproductive glands gene. Sfp genes with reproductive-tissue-specific expression were enriched for both directional and stabilizing selection, while relaxed selection was the predominant mode of evolution among Sfp genes with any other nonreproductive tissue-specific or nontissue-specific expression. The knockdown of single genes known to affect intraspecific sperm competition, and with patterns of expression divergence and polymorphism suggestive of directional selection, was not enough to break down postmating reproductive isolation barriers between species. Our results identify the expression of male-specific Sfp genes as an enriched target of selection and suggest a complex molecular relationship between postcopulatory sexual selection on a single gene's expression and its effect on the onset of speciation.

Gametic selection favours polyandry and selfing.

Competition among pollen or sperm (gametic selection) can cause evolution. Mating systems shape the intensity of gametic selection by determining the competitors involved, which can in turn cause the mating system itself to evolve. We model the bidirectional relationship between gametic selection and mating systems, focusing on variation in female mating frequency (monandry-polyandry) and self-fertilisation (selfing-outcrossing). First, we find that monandry and selfing both reduce the efficiency of gametic selection in removing deleterious alleles. This means that selfing can increase mutation load, in contrast to cases without gametic selection where selfing purges deleterious mutations and decreases mutation load. Second, we explore how mating systems evolve via their effect on gametic selection. By manipulating gametic selection, polyandry can evolve to increase the fitness of the offspring produced. However, this indirect advantage of post-copulatory sexual selection is weak and is likely to be overwhelmed by any direct fitness effects of mating systems. Nevertheless, gametic selection can be potentially decisive for selfing evolution because it significantly reduces inbreeding depression, which favours selfing. Thus, the presence of gametic selection could be a key factor driving selfing evolution.

Contrasting the form and strength of pre- and postcopulatory sexual selection in a flatworm.

Sexual traits may be selected during multiple consecutive episodes of selection, occurring before, during, or after copulation. The overall strength and form of selection acting on traits may thus be determined by how selection (co-)varies along different episodes. However, it is challenging to measure pre- and postcopulatory phenotypic traits alongside variation in fitness components at each different episode. Here, we used a transgenic line of the transparent flatworm Macrostomum lignano expressing green fluorescent protein (GFP) in all cell types, including sperm cells, enabling in vivo sperm tracking. We assessed the mating success, sperm-transfer efficiency, and sperm fertilizing efficiency of GFP(+) focal worms in which we measured 13 morphological traits. We found linear selection on sperm production rate arising from pre- and postcopulatory components and on copulatory organ shape arising from sperm fertilizing efficiency. We further found nonlinear (mostly concave) selection on combinations of copulatory organ and sperm morphology traits arising mostly from sperm-transfer efficiency and sperm fertilizing efficiency. Our study provides a fine-scale quantification of sexual selection, showing that both the form and strength of selection can change across fitness components. Quantifying how sexual selection builds up along episodes of selection allows us to better understand the evolution of sexually selected traits.

Do male reproductive traits evolve at the intraspecific level in response to the amount of placentotrophy in a genus of viviparous fishes?

Placentotrophy is a particular type of maternal provisioning to developing embryos, in which mothers actively provide nutrients via complex placental structures. Placentotrophy implies less pre-fertilization investment, resulting in a shift from pre- to post-copulatory sexual selection. This change can potentially result in a conflict between females and males. This phenomenon has been demonstrated at the interspecific level in viviparous fishes of the family Poeciliidae, in which males of species that lack placentotrophy have evolved traits related to pre-copulatory sexual selection such as coloration, ornaments, and courtship behavior. Placentotrophic species, on the other hand, have evolved traits associated with post-copulatory sexual selection such as long intromittent organs (gonopodium) and increased sexual coercion behavior. Here we test, for the first time at the intraspecific level, whether there is a similar relationship between a higher degree of female placentotrophy and the evolution of male reproductive traits (larger testes and longer gonopodia) in three species of the genus Poeciliopsis (P. gracilis, P. infans, and P. prolifica). We observed a tendency towards longer gonopodia in males of P. gracilis as well as the largest testes of P. prolifica males in the populations with the highest degrees of placentotrophy. However, the statistical support for these findings was relatively weak. Therefore, we failed to support the hypothesis of a selective effect of female placentotrophy on male gonads and genitalia. We discuss other evolutionary forces that may have driven the observed intraspecific variation in male reproductive traits of Poeciliopsis fishes.

Sperm production is negatively associated with muscle and sperm telomere length in a species subjected to strong sperm competition.

Life-history theory suggests that ageing is one of the costs of reproduction. Accordingly, a higher reproductive allocation is expected to increase the deterioration of both the somatic and the germinal lines through enhanced telomere attrition. In most species, males' reproductive allocation mainly regards traits that increase mating and fertilization success, that is sexually selected traits. In this study, we tested the hypothesis that a higher investment in sexually selected traits is associated with a reduced relative telomere length (RTL) in the guppy (Poecilia reticulata), an ectotherm species characterized by strong pre- and postcopulatory sexual selection. We first measured telomere length in both the soma and the sperm over guppies' lifespan to see whether there was any variation in telomere length associated with age. Second, we investigated whether a greater investment in pre- and postcopulatory sexually selected traits is linked to shorter telomere length in both the somatic and the sperm germinal lines, and in young and old males. We found that telomeres lengthened with age in the somatic tissue, but there was no age-dependent variation in telomere length in the sperm cells. Telomere length in guppies was significantly and negatively correlated with sperm production in both tissues and life stages considered in this study. Our findings indicate that telomere length in male guppies is strongly associated with their reproductive investment (sperm production), suggesting that a trade-off between reproduction and maintenance is occurring at each stage of males' life in this species.

Population‐level food availability affects postcopulatory sexual selection dynamics in the guppy

Abstract Postcopulatory sexual selection (PCSS), namely sperm competition and cryptic female choice, is typically investigated in benign environments, with a fixed number of partners, which mate at the same time intervals; all conditions that are rarely met in natural populations. Although there is increasing evidence that environmental fluctuations affect sexual selection before mating, whether and to which extent they influence postcopulatory trajectories is still little explored. PCSS was investigated in replicate populations of guppies (Poecilia reticulata) in which males and females mated after maintained for 2 weeks on either restricted (RE) or ad libitum (AL) diet and the paternity of the offspring produced by multiply mated females was assigned using microsatellite markers. Compared to AL fish, RE females (i) had fewer mating partners, but the time interval between the first and the last mating was not affected; (ii) produced broods with a lower variance in male fertilization success (a measure of the opportunity for PCSS); and (iii) produced broods with a paternity bias towards the first mate (reversing the last sperm precedence observed in AL populations), and associated more towards males with higher courtship rate. Our results demonstrate that short‐term limitation in food availability significantly influence PCSS by modifying both fertilization success variance and sperm precedence pattern. Environmental variation should therefore become part of the research paradigm to improve our understanding of postcopulatory evolutionary dynamics. Read the free Plain Language Summary for this article on the Journal blog.

Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection.

In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al., PLoS One, 11, 2016, e0154468), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provides information on each focal male's mating order and the frequency in which focal males remated with same females ('repetitive matings'). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences.

X chromosome drive is constrained by sexual selection and influences ornament evolution.

Experimental evolution provides an integrative method for revealing complex interactions among evolutionary processes. One such interaction involves sex-linked selfish genetic elements and sexual selection. X-linked segregation distorters, a type of selfish genetic element, influence sperm transmission to increase in frequency and consequently alter the population sex ratio and the opportunity for sexual selection, while sexual selection may impact the spread of X-linked distorters. Here we manipulated sexual selection by controlling female mating opportunities and the presence of a distorting X chromosome in experimental lines of the stalk-eyed fly, Teleopsis dalmanni, over 11 generations. We find that removal of sexual selection leads to an increase in the frequency of the X-linked distorter and sex ratio across generations and that post-copulatory sexual selection alone is sufficient to limit the frequency of distorters. In addition, we find that male eyestalk length, a trait under pre-copulatory sexual selection, evolves in response to changes in the strength of sexual selection with the magnitude of the response dependent on X chromosome type and the frequency of distorting X chromosomes. These results reveal how a selfish X can interact with sexual selection to influence the evolution of sexually selected traits in multiple ways.

The impact of small groups on pre- and postcopulatory sexual selection in polyandrous populations.

Sexual selection is a key evolutionary force but varies widely between populations. Two key factors that influence sexual selection are the extent to which females copulate with multiple males (polyandry) and variation in the social environment. Increasing research demonstrates populations are structured by complex socio-sexual networks, and the structure of these networks can influence sexual selection by shaping the relationship between male precopulatory mating success and the intensity of postcopulatory competition. However, comparatively less attention has been dedicated to the influence of group structure on sexual selection and how differences in the size of groups may impact on the relative force of pre- and postcopulatory sexual selection in polyandrous populations. The presence of groups (i.e., group structure) and the size of groups varies widely in nature and forms an implicit part of much experimental sexual selection research under laboratory conditions. Here I use simulations of mating competition within populations that vary in the size of groups they contain, to show that variation in group size, and in particular small groups, can influence sexual selection. Specifically, I show that null expectations for the operation of pre- and postcopulatory sexual selection is governed by the size of groups within populations because smaller group sizes constrain the structure of sexual networks leading to reinforcing episodes of pre- and postcopulatory sexual selection. Given broad variation in group structure in nature and the tendency for experimental sexual selection research to study replicate small groups, these effects have implications for our understanding of the operation of sexual selection in polyandrous populations.

Heat stress reveals a fertility debt owing to postcopulatory sexual selection.

Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We first adopted a classic life history theory framework, incorporating a trade-off between reproduction and maintenance, and applied it to the male germline to generate formalized predictions for how an evolutionary history of strong postcopulatory sexual selection (sperm competition) may affect male fertility under acute adult heat stress. We then tested these predictions by assessing the thermal sensitivity of fertility (TSF) in replicated lineages of seed beetles maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. In line with the theoretical predictions, we find that males evolving under strong sexual selection suffer from increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under immediate risk during extreme heat waves expected under future climate change.

Examining the potential for resource-dependent female reproductive fluid-sperm interactive effects in a livebearing fish.

Sexually selected traits can be costly to produce and maintain. The amount of resources available to an individual is therefore expected to influence investment in costly sexual traits. While resource-dependent expression of sexually selected traits has traditionally been examined in males, resource limitation can also influence how sexual selection operates in females. Female reproductive fluids are thought to be costly to produce and may play an important role in shaping the outcome of postcopulatory sexual selection by influencing sperm performance. However, we know surprisingly little about whether and how female reproductive fluids are influenced by resource limitation. Here, we examine if resource restriction influences female reproductive fluid-sperm interactive effects in the pygmy halfbeak (Dermogenys collettei), a small internally fertilizing freshwater fish where females store sperm. After experimentally altering female diets (high vs. restricted diets), we compared how female reproductive fluids influence two key metrics of sperm quality: sperm viability and velocity. While female reproductive fluids enhanced sperm viability and velocity, we found no evidence that female diet influenced the interactive effect between female reproductive fluids and sperm viability or velocity. Our findings build on the growing evidence that female reproductive fluids influence sperm performance and call for further attention to be devoted to understanding how resource quantity and quality influence how female reproductive fluids affect sperm performance.

Disentangling the causes of temporal variation in the opportunity for sexual selection

In principle, temporal fluctuations in the potential for sexual selection can be estimated as changes in intrasexual variance in reproductive success (i.e. the opportunity for selection). However, we know little about how opportunity measures vary over time, and the extent to which such dynamics are affected by stochasticity. We use published mating data from multiple species to investigate temporal variation in the opportunity for sexual selection. First, we show that the opportunity for precopulatory sexual selection typically declines over successive days in both sexes and shorter sampling periods lead to substantial overestimates. Second, by utilising randomised null models, we also find that these dynamics are largely explained by an accumulation of random matings, but that intrasexual competition may slow temporal declines. Third, using data from a red junglefowl (Gallus gallus) population, we show that declines in precopulatory measures over a breeding period were mirrored by declines in the opportunity for both postcopulatory and total sexual selection. Collectively, we show that variance-based metrics of selection change rapidly, are highly sensitive to sampling durations, and likely lead to substantial misinterpretation if used as indicators of sexual selection. However, simulations can begin to disentangle stochastic variation from biological mechanisms.

How Female-Female Competition Affects Male-Male Competition: Insights into Postcopulatory Sexual Selection from Socially Polyandrous Species.

AbstractSexual selection is a major driver of trait variation, and the intensity of male competition for mating opportunities has been linked with sperm size across diverse taxa. Mating competition among females may also shape the evolution of sperm traits, but the effect of the interplay between female-female competition and male-male competition on sperm morphology is not well understood. We evaluated variation in sperm morphology in two species with socially polyandrous mating systems, in which females compete to mate with multiple males. Northern jacanas (Jacana spinosa) and wattled jacanas (J. jacana) vary in their degree of social polyandry and sexual dimorphism, suggesting species differences in the intensity of sexual selection. We compared mean and variance in sperm head, midpiece, and tail length between species and breeding stages because these measures have been associated with the intensity of sperm competition. We found that the species with greater polyandry, northern jacana, has sperm with longer midpieces and tails as well as marginally lower intraejaculate variation in tail length. Intraejaculate variation was also significantly lower in copulating males than in incubating males, suggesting flexibility in sperm production as males cycle between breeding stages. Our results indicate that stronger female-female competition for mating opportunities may also shape more intense male-male competition by selecting for longer and less variable sperm traits. These findings extend frameworks developed in socially monogamous species to reveal that sperm competition may be an important evolutionary force layered atop female-female competition for mates.

A novel method to collect sperm from brood parasitic cuckoos: Urodeum stimulation (UroS) method

Sperm competition has been studied in numerous species as a representative example of postcopulatory sexual selection, where sampling sperm from male is the most basic and important step. Sperm collection can be tricky in birds, however, because unlike mammals, the genitals of birds are generally latent in the cloacal region and their characteristics vary among species. Various methods to collect sperm from different birds have been tested, such as cloacal massage, feces collection, and electro-stimulation, but their applicability varies depending on species. In this study, we introduced the urodeum stimulation method (UroS method) to collect sperm from Cuculus cuckoos, such as the Common Cuckoo (C. canorus). These species are expected to have interesting patterns of pair bonding and sperm competition because of their unique breeding strategy called brood parasitism; however, it remains unexplored. In this study, we described the application of our new method to expel semen from male common cuckoos, measured the volume of semen collected, checked the presence of sperm in the semen sample, and finally estimated its success rate among 82 males. Samples were successfully collected from 76 cuckoos (approximately 93%) and the colors and volumes of the samples were very diverse. Sperm was present in 43 of these samples (57%), showing a sperm observation rate approximately twice as high as that of the conventional cloacal massage method. We believe that this novel method will contribute to a better understanding of postcopulatory sexual selection in avian brood parasites and facilitate the process of sperm collection and artificial insemination in other medium-sized birds.

Pre- and post-copulatory sexual selection increase offspring quality but impose survival costs to female field crickets.

Whether sexual selection increases or decreases fitness is under ongoing debate. Sexual selection operates before and after mating. Yet, the effects of each episode of selection on individual reproductive success remain largely unexplored. We ask how disentangled pre- and post-copulatory sexual selection contribute to fitness of field crickets Gryllus bimaculatus. Treatments allowed exclusively for (i) pre-copulatory selection, with males fighting and courting one female, and the resulting pair breeding monogamously, (ii) post-copulatory selection, with females mating consecutively to multiple males and (iii) relaxed selection, with enforced pair monogamy. While standardizing the number of matings, we estimated a number of fitness traits across treatments and show that females experiencing sexual selection were more likely to reproduce, their offspring hatched sooner, developed faster and had higher body mass at adulthood, but females suffered survival costs. Interestingly, we found no differences in fitness of females or their offspring from pre- and post-copulatory sexual selection treatments. Our findings highlight the potential for sexual selection in enhancing indirect female fitness while concurrently imposing direct survival costs. By potentially outweighing these costs, increased offspring quality could lead to beneficial population-level consequences of sexual selection.