Precopulatory Sexual Selection Research Articles

Behavioral estimates of mating success corroborate genetic evidence for pre-copulatory selection

Abstract In promiscuous species, fitness estimates obtained from genetic parentage may often reflect both pre- and post-copulatory components of sexual selection. Directly observing copulations can help isolate the role of pre-copulatory selection, but such behavioral data are difficult to obtain in the wild and may also overlook post-copulatory factors that alter the relationship between mating success and reproductive success. To overcome these limitations, we combined genetic parentage analysis with behavioral estimates of size-specific mating in a wild population of brown anole lizards (Anolis sagrei). Males of this species are twice as large as females and multiple mating among females is common, suggesting the scope for both pre- and post-copulatory processes to shape sexual selection on male body size. Our genetic estimates of reproductive success revealed strong positive directional selection for male size, which was also strongly associated with the number of mates inferred from parentage. In contrast, a male’s size was not associated with the fecundity of his mates or his competitive fertilization success. By simultaneously tracking copulations in the wild via the transfer of colored powder to females by males from different size quartiles, we independently confirmed that large males were more likely to mate than small males. We conclude that body size is primarily under pre-copulatory sexual selection in brown anoles, and that post-copulatory processes do not substantially alter the strength of this selection. Our study also illustrates the utility of combining both behavioral and genetic methods to estimate mating success to disentangle pre- and post-copulatory processes in promiscuous species.

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.

Evidence for stronger sexual selection in males than females using an adapted method of Bateman's classic study of Drosophila melanogaster.

Bateman's principles, originally a test of Darwin's theoretical ideas, has since become fundamental to sexual selection theory and vital to contextualising the role of anisogamy in sex differences of precopulatory sexual selection. Despite this, Bateman's principles have received substantial criticism, and researchers have highlighted both statistical and methodological errors, suggesting that Bateman's original experiment contains too much sampling bias for there to be any evidence of sexual selection. This study uses Bateman's original method as a template, accounting for two fundamental flaws in his original experiments, (i) viability effects and (ii) a lack of mating behaviour observation. Experimental populations of Drosophila melanogaster consisted of wild-type focal individuals and non-focal individuals established by backcrossing the brown eye (bw -) eye-colour marker - thereby avoiding viability effects. Mating assays included direct observation of mating behaviour and total number of offspring, to obtain measures of mating success, reproductive success, and standardised variance measures based on Bateman's principles. The results provide observational support for Bateman's principles, particularly that (i) males had significantly more variation in number of mates compared to females and (ii) males had significantly more individual variation in total number of offspring. We also find significantly steeper Bateman gradient for males compared to females, suggesting that sexual selection is operating more intensely in males. However, female remating was limited, providing the opportunity for future study to further explore female reproductive success in correlation with higher levels of remating.

A clear-cut difference in nuptial strategies may shape sperm traits in two paper wasps

Abstract Spermatozoa vary in quantity, quality and design across species and individuals. Here, we reported the first detailed analysis of sperm traits in two primitively eusocial paper wasps, Polistes dominula and Polistes gallicus, which differ in their nuptial strategies and body size as follows: lek-territoriality of the large P. dominula males, defending exclusive territories at landmarks; scramble competition of the small P. gallicus, where serial mating may occur because males interfere with rivals and replace them during copulation. We compared the number, viability, and length of sperm, and its coefficient of variation, between these sympatric paper wasps patrolling and marking the same landmarks during the same summer: a good opportunity to analyse sperm across species while controlling for environmental variables. Spermatozoa were more numerous and longer in P. dominula than in P. gallicus males. Viability was similar in both species and positively covaried with male body size. Intra-male variation in sperm length was significantly reduced in P. gallicus, as predicted in the case of selection for an optimal sperm design. We hypothesized that precopulatory sexual selection (lek-territoriality vs. scramble competition) may affect sperm traits.

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.

Mating assortment and the strength of sexual selection in a polyandrous population of Cook Strait giant weta

AbstractPolyandry can profoundly affect the strength of pre-copulatory sexual selection acting on males because each additional mate acquired by a female means that, all else being equal, a male’s paternity share declines. However, accruing additional mates could benefit male fitness if males with greater mating success also tend to have less promiscuous females as partners. If this is indeed the case, then males should experience strong sexual selection to acquire more mates. We tested these predictions by collecting detailed mating data on male and female Cook Strait giant weta (Deinacrida rugosa) in the wild via daily radio tracking. Our sexual network-based approach indeed revealed that the most polygynous male D. rugosa mated the least polyandrous females. This finding therefore suggests that the most successful males likely face lower intensities of sperm competition and so should be selected to accrue more mates. Further, our selection analysis revealed significant pre-copulatory sexual selection on males with those having relatively smaller body size, lighter body mass, and longer legs accruing more mates than otherwise. Thus, it appears that both pre- and post-copulatory episodes of sexual selection reinforce the same male phenotype.

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.

Genetic link between mobility and sexual attractiveness in male Tribolium castaneum beetles

Securing females is a crucial determinant of male fitness in many species. Mate-searching efficiency is often associated with increased mobility in males, but an increased investment in movement may reduce other fitness traits via potential trade-offs. In precopulatory sexual selection via female mate choice, the rate of encounter with females and the attractiveness of males are essential to increase male mating success. If there is a trade-off between mobility and attractiveness in males, males with higher mobility may show lower attractiveness. We here assessed whether artificial selection of mobility affected male attractiveness in the red flour beetle, Tribolium castaneum . We compared the olfactory attractiveness of males (due to 4,8-dimethyldecanal) between strains having genetically higher mobility or lower mobility. The results indicated that females were significantly more attracted to the odours of lower mobility males. Therefore, our results suggested that a genetic trade-off might have occurred between mobility and attractiveness in males. This cost–benefit balance may lead to the maintenance of individual differences in mobility within a population. • Males of the red flour beetle release a pheromone to attract females. • Artificial selection for mobility had established high- and low-mobility strains. • A trade-off exists between adult mobility and male attractiveness. • Males of the low-mobility strain achieve mating by a chemical attraction strategy.

Is plasticity in field cricket mating behaviour mediated by experience of song quality?

Many animals rely upon signals to discriminate among potential mates. Through mate choice, they may gain fitness advantages for themselves and their offspring and exert selection on signals and signallers. In some species, mating preferences are phenotypically plastic and mediated by experience of signals. Teleogryllus oceanicus , the Pacific field cricket, has been a productive model for studies of acoustically mediated phenotypic plasticity because many aspects of adult mating behaviour and reproductive physiology are differentially expressed when crickets develop in the presence versus absence of conspecific signals. An open question is whether the quality of conspecific signals experienced during development also mediates the mating preferences of adult females, as it does in some other animals. We tested the mating assurance in a variable environment hypothesis, which posits that adaptive plasticity in the expression of female mating preferences could protect females from costs associated with being too selective when preferred mates are rare or absent, while allowing selectivity when preferred mates are available. We experimentally manipulated the acoustic signals in the rearing environment as a reliable cue about the availability of preferred mates in the adult environment. Specifically, environments varied in the percentage of long chirp, a trait of male advertisement song known to be under precopulatory sexual selection. When subjects reached maturity, we used a within-subjects phonotaxis (movement towards sound) assay to measure female preferences for the percentage of long chirp. We replicated our experiment in populations from three islands of the Hawaiian Archipelago. We found evidence that some measures of female response are plastic and mediated by song quality, but effects were population specific and not entirely consistent with the predictions of the mating assurance in a variable environment hypothesis. Our results point to limited song quality-mediated plasticity in female mating preferences. • We manipulated signal quality in the environment and measured phonotaxis behaviour. • Plasticity in female mating behaviour was limited and variable among populations. • Oʻahu females were more responsive, selective after experiencing high-quality song. • Hilo females showed a peak preference for 60% long chirp songs and no plasticity. • Kauaʻi, a population with near-complete signal loss, showed no song preference.

Sperm Numbers as a Paternity Guard in a Wild Bird.

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.

Male fattening is related to increased seminal quality of squirrel monkeys (Saimiri collinsi): Implications for sperm competition.

Saimiri are neotropical primates with seasonal reproduction, males develop a seasonal fattening condition that has been suggested as a pre-copulatory sexual selection strategy. Furthermore, females mate with multiple males in the same season. This could also favor the evolution of a postcopulatory sexual strategy by sperm competition. In this study, we tested the hypothesis that there is a relationship between the fatted condition and advantageous seminal characteristics in Saimiri collinsi and evaluated its implications for sperm competition. Adult males (N = 10), aged 5-15 years, housed in mixed or only-male groups, were analyzed from June, 2015 to July, 2016. Measurements of weight, axilla, and arm skinfold, and testicular volume were taken monthly, and semen was collected by electroejaculation. A fattening index was developed to quantify and identify fatted males, biometrics, and seminal parameters were compared between the non-fatted and fatted conditions. The fatted males present a larger testicular volume. This is related to the increase in spermatogenic activity necessary to sustain a high ejaculation frequency during the mating season. An increase in seminal volume and in frequency of semen coagulation were detected in fatted males, advantages related to sperm protection in the female reproductive tract. Age and social context were not significant sources of variation for both morphological and seminal traits. A decrease in response from the fatted males in obtaining semen and an increase in the frequency of azoospermic ejaculates were observed. These unexpected results may be due to intense reproductive activities in a short period. The fattening phenomenon has many implications in the sexual selection of squirrel monkeys, and they are still not entirely unveiled. Our results corroborate the idea that, in S. collinsi, the fatted male condition is related to sexual selection, and we found evidence suggesting it may be also expressed by a post-copulatory component, sperm competition.

Sexual selection and sexual size dimorphism in animals.

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.

Female reproductive mode shapes allometric scaling of male traits in live-bearing fishes (family Poeciliidae).

Reproductive mode is predicted to influence the form of sexual selection. The viviparity-driven conflict hypothesis posits that a shift from lecithotrophic (yolk-nourished) to matrotrophic (mother-nourished or placental) viviparity drives a shift from precopulatory towards post-copulatory sexual selection. In lecithotrophic species, we predict that precopulatory sexual selection will manifest as males exhibiting a broad distribution of sizes, and small and large males exhibiting contrasting phenotypes (morphology and coloration); conversely, in matrotrophic species, an emphasis on post-copulatory sexual selection will preclude these patterns. We test these predictions by gathering data on male size, morphology and coloration for five sympatric Costa Rican poeciliid species that differ in reproductive mode (i.e. lecithotrophy vs. matrotrophy). We find tentative support for these predictions of the viviparity-driven conflict hypothesis, with some interesting caveats and subtleties. In particular, we find that the three lecithotrophic species tend to show a broader distribution of male sizes than matrotrophic species. Furthermore, large males of such species tend to exhibit proportionately large dorsal and caudal fins and short gonopodia relative to small males, while these patterns are expressed to a lesser extent in the two matrotrophic species. Finally, large males in some of the lecithotrophic species exhibit darker fins relative to small males, a pattern not evident in either matrotrophic species. One unexpected finding was that even in the matrotrophic species Poeciliopsis retropinna and Poeciliopsis paucimaculata, which lack courtship and dichromatic coloration, some morphological traits exhibit significant allometric relationships, suggesting that even in these species precopulatory sexual selection may be present and shaping size-specific male phenotypes in subtle ways.

Comparative sexual selection in field and laboratory in a guild of sepsid dung flies

Phenomenological and behavioural studies have greatly advanced the study of natural selection. Field studies of selection well appraise the natural situation, but is this also true for laboratory studies, which are typically more mechanistic? We compared precopulatory sexual selection (mating differential based on pairing success) in field and laboratory of several closely related, ecologically similar black scavenger dung flies (Diptera: Sepsidae). Selection on fore femur (sexual trait) and wing size (nonsexual trait) and shape varied considerably among seven species and continental populations in agreement with variation in their mating system and sexual size dimorphism. Selection on trait size was mostly positive or nil, but never significantly negative, implying mating advantages of large males in most species. Strongest selection was found in species/populations with male-biased size dimorphism, associating evolutionary shifts from female- to male-biased dimorphism with intensified sexual selection for large male size by adding male –male competition to a mating system previously driven primarily by female choice. Although sexual selection on shape was closely aligned with allometric shape variation, selection on fore femur shape was more consistent than selection on wing shape, which was absent in most species. Sexual selection intensities, but not necessarily the underlying behavioural mechanisms, were overall similar in field and laboratory, suggesting that laboratory assessments well represent the natural situation. If this conclusion can be generalized, it would lend credence to the strategy of using controlled laboratory mating studies to better understand natural selection, behaviour and ecology, at least for smaller animals that can be held in captivity.

How Soon Hath Time… A History of Two "Seminal" Publications.

This review documents the history of the two papers written half a century ago that relate to this special issue of Cells. The first, “Sperm competition and its evolutionary consequences in the insects” (Biological Reviews, 1970), stressed that sexual selection continues after ejaculation, resulting in many adaptations (e.g., postcopulatory guarding phases, copulatory plugs, seminal fluid components that modify female reproduction, and optimal ejaculation strategies), an aspect not considered by Darwin in his classic treatise of 1871. Sperm competition has subsequently been studied in many taxa, and post-copulatory sexual selection is now considered an important sequel to Darwinian pre-copulatory sexual selection. The second, “The origin and evolution of gamete dimorphism and the male-female phenomenon” (Journal of Theoretical Biology, 1972) showed how selection, based on gamete competition between individuals, can give rise to anisogamy in an isogamous broadcast spawning ancestor. This theory, which has subsequently been developed in various ways, is argued to form the most powerful explanation of why there are two sexes in most multicellular organisms. Together, the two papers have influenced our general understanding of the evolutionary differentiation of the two forms of gametic cells, and the divergence of sexual strategies between males and females under sexual selection.

Combined effects of rearing and testing temperatures on sperm traits.

Temperature experienced during early development can affect a range of adult life-history traits. Animals often show seemingly adaptive developmental plasticity-with animals reared at certain temperatures performing better as adults at those temperatures. The extent to which this type of adaptive response occurs in gonadal tissue that affects sperm traits is, however, poorly studied. We initially reared male mosquito fish (Gambusia holbrooki) at either 18°C or 30°C, and then measured their sperm reserves as adults. We also looked at the velocity of their sperm, at both the matched and mismatched temperatures. Although males reared at 30°C were larger than those initially reared at 18°C, there was no detectable effect of rearing temperature on absolute sperm number. Sperm swam faster at 30°C than 18°C regardless of the male's rearing temperature. Therefore, we found no evidence of adaptive developmental plasticity. Rearing temperature did, however, significantly influence the relationship between male body size and sperm velocity. Larger males had faster sperm when reared at the warmer temperature and slower sperm when reared at the cooler temperature. This suggests that rearing temperature could alter the relationship between pre-copulatory sexual selection and post-copulatory sexual selection as male size affects mating success. Finally, there was a positive correlation between velocities at the two test temperatures, suggesting that temperature experienced during sperm competition is unlikely to affect a male's relative fertilization success.

The importance of pre- and postcopulatory sexual selection promoting adaptation to increasing temperatures.

Global temperatures are increasing rapidly affecting species globally. Understanding if and how different species can adapt fast enough to keep up with increasing temperatures is of vital importance. One mechanism that can accelerate adaptation and promote evolutionary rescue is sexual selection. Two different mechanisms by which sexual selection can facilitate adaptation are pre- and postcopulatory sexual selection. However, the relative effects of these different forms of sexual selection in promoting adaptation are unknown. Here, we present the results from an experimental study in which we exposed fruit flies Drosophila melanogaster to either no mate choice or 1 of 2 different sexual selection regimes (pre- and postcopulatory sexual selection) for 6 generations, under different thermal regimes. Populations showed evidence of thermal adaptation under precopulatory sexual selection, but this effect was not detected in the postcopulatory sexual selection and the no choice mating regime. We further demonstrate that sexual dimorphism decreased when flies evolved under increasing temperatures, consistent with recent theory predicting more sexually concordant selection under environmental stress. Our results suggest an important role for precopulatory sexual selection in promoting thermal adaptation and evolutionary rescue.

No evidence of male-biased sexual selection in a snake with conventional Darwinian sex roles.

Decades of research on sexual selection have demonstrated that ‘conventional’ Darwinian sex roles are common in species with anisogamous gametes, with those species often exhibiting male-biased sexual selection. Yet, mating system characteristics such as long-term sperm storage and polyandry have the capacity to disrupt this pattern. Here, these ideas were explored by quantifying sexual selection metrics for the western diamond-backed rattlesnake (Crotalus atrox). A significant standardized sexual selection gradient was not found for males (βSS = 0.588, p = 0.199) or females (βSS = 0.151, p = 0.664), and opportunities for sexual selection (Is) and selection (I) did not differ between males (Is = 0.069, I = 0.360) and females (Is = 0.284, I = 0.424; both p > 0.05). Furthermore, the sexes did not differ in the maximum intensity of precopulatory sexual selection (males: s′max = 0.155, females: s′max = 0.080; p > 0.05). Finally, there was no evidence that male snout–vent length, a trait associated with mating advantage, is a target of sexual selection (p > 0.05). These results suggest a lack of male-biased sexual selection in this population. Mating system characteristics that could erode male-biased sexual selection, despite the presence of conventional Darwinian sex roles, are discussed.

Experimental evidence for accelerated adaptation to desiccation through sexual selection on males.

The impact of sexual selection on the adaptive process remains unclear. On the one hand, sexual selection might hinder adaptation by favouring costly traits and preferences that reduce nonsexual fitness. On the other hand, condition dependence of success in sexual selection may accelerate adaptation. Here, we used replicate populations of Drosophila melanogaster to artificially select on male desiccation resistance while manipulating the opportunity for precopulatory sexual selection in a factorial design. Following five generations of artificial selection, we measured the desiccation resistance of males and females to test whether the addition of sexual selection accelerated adaptation. We found a significant interaction between the effects of natural selection and sexual selection: desiccation resistance was highest in populations where sexual selection was allowed to operate. Despite only selecting on males, we also found a correlated response in females. These results provide empirical support for the idea that sexual selection can accelerate the rate of adaptation.

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male-male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S.neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male-male competition. We predicted that populations subject to increased male-male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male-biased SSD in both species, which was not evident in conspecific populations with female-biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.