Opportunity For Sexual Selection Research Articles

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.

Extra-pair paternity and sexual dimorphism in birds.

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.

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.

Sex ratio effects on reproductive success of male and female Daphnia.

The intensity of mating competition and the opportunity for sexual selection are thought to depend on the operational sex ratio, the ratio of sexually active males to fertilizable females. Cyclic parthenogens, organisms that alternate between sexual reproduction and female-only parthenogenesis, show particularly high variation in sex ratios in natural populations but the effects of this variation on mating competition and reproductive success of each sex are poorly understood. In a series of experiments with Daphnia magna, we experimentally imposed five sex ratio categories, varying from one male per 81 females to an even sex ratio. We found that, in males, reproductive success strongly and monotonically decreased with decreasing number of females per male. In females, in contrast, mating success and reproductive success were reduced only at the most female-biased sex ratio (1:81), when many females remained unmated and unfertilized, and then again at equal sex ratios, probably due to negative effects of high density or stress induced by numerous males. Our results suggest that females experienced male limitation at heavily female-biased sex ratios below one male to about 50 females. As this is well within the sex ratio variation observed in natural Daphnia populations, we conclude that mating competition and the opportunity for sexual selection may exist not only in males but, at least periodically, also in females.

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.

Mating systems and predictors of relative reproductive success in a Cutthroat Trout subspecies of conservation concern.

Mating systems and patterns of reproductive success in fishes play an important role in ecology and evolution. While information on the reproductive ecology of many anadromous salmonids (Oncorhynchus spp.) is well detailed, there is less information for nonanadromous species including the Yellowstone Cutthroat Trout (O. clarkii bouvieri), a subspecies of recreational angling importance and conservation concern. Using data from a parentage‐based tagging study, we described the genetic mating system of a migratory population of Yellowstone Cutthroat Trout, tested for evidence of sexual selection, and identified predictors of mating and reproductive success. The standardized variance in mating success (i.e., opportunity for sexual selection) was significantly greater for males relative to females, and while the relationship between mating success and reproductive success (i.e., Bateman gradient) was significantly positive for both sexes, a greater proportion of reproductive success was explained by mating success for males (r 2 = 0.80) than females (r 2 = 0.59). Overall, the population displayed a polygynandrous mating system, whereby both sexes experienced variation in mating success due to multiple mating, and sexual selection was variable across sexes. Tests for evidence of sexual selection indicated the interaction between mating success and total length best‐predicted relative reproductive success. We failed to detect a signal of inbreeding avoidance among breeding adults, but the group of parents that produced progeny were on average slightly less related than adults that did not produce progeny. Lastly, we estimated the effective number of breeders (N b) and effective population size (N e) and identified while N b was lower than N e, both are sufficiently high to suggest Yellowstone Cutthroat Trout in Burns Creek represent a genetically stable and diverse population.

Rainfall decrease and red deer rutting behaviour: Weaker and delayed rutting activity though higher opportunity for sexual selection.

In the last decades, climate change has caused an increase in mean temperatures and a reduction in average rainfall in southern Europe, which is expected to reduce resource availability for herbivores. Resource availability can influence animals' physical condition and population growth. However, much less is known on its effects on reproductive performance and sexual selection. In this study, we assessed the impact of three environmental factors related to climate change (rainfall, temperature and vegetation index) on Iberian red deer Cervus elaphus hispanicus reproductive timing and sexual behaviour, and their effects on the opportunity for sexual selection in the population. We measured rutting phenology as rut peak date, the intensity of male rutting activity as roaring rate, and the opportunity for sexual selection from the distribution of females among harem holding males in Doñana Biological Reserve (Southwest Spain), from data of daily observations collected during the rut over a period of 25 years. For this study period, we found a trend for less raining and hence poorer environmental conditions, which associated with delayed rutting season and decreased rutting intensity, but that appeared to favour a higher degree of polygyny and opportunity for sexual selection, all these relationships being modulated by population density and sex ratio. This study highlights how climate change (mainly rainfall reduction in this area) can alter the conditions for mating and the opportunity for sexual selection in a large terrestrial mammal.

Male condition and group heterogeneity predict extra-group paternity in a Neotropical bat

Extra-group paternity, in which offspring are sired by a male outside the breeding group, may alter the distribution of reproductive success in a population, thus affecting the opportunity for sexual selection. Both inter- and intraspecific studies have focused largely on mating systems in which females choose their social mates, and less is known about extra-group paternity in polygynous systems in which social mates are largely dictated by male-male competition. In this study, we examine the frequency and distribution of extra-group paternity in a harem-forming bat, Phyllostomus hastatus. We find that despite aggressive harem defense, males are unable to fully monopolize reproduction within their harem and over 70% of harems contain extra-group offspring. Harem males in better body condition suffered less paternity loss, but we found no effect of male age or body size. Even though the age and size of individual females did not predict offspring paternity, we found a significant effect of age heterogeneity within the group. Harems composed of differently aged females were more likely to contain extra-group offspring. Our results not only provide evidence for the role of male defense in preventing extra-group paternity but also suggest that social group composition has consequences for male reproductive success. In polygynous societies, the ability to monopolize mating is critical to reproductive success. As the group size increases, defense often becomes more difficult, resulting in increased rates of extra-group paternity. We find that among greater spear-nosed bats, extra-group offspring occur in most harems, but the overall rate of extra-group paternity is relatively low despite their large harems (15–30 females). Variation in the rate of extra-group paternity between harems is explained by male body condition (i.e., relative mass) but not harem size. Additionally, the rate of extra-group paternity is not explained entirely by male attributes, as we find that age heterogeneity within the female group is a significant predictor of the extra-group paternity rate. Our results support the hypothesis that not only the physical condition of a male influences his ability to monopolize reproduction but also the group composition influences the female mating behavior.

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.

Variance in lifetime reproductive success of male polar bears

Abstract Despite the important role that population density plays in ecological and evolutionary processes, studies of solitary species that occur at low densities remain scarce. In the context of mating systems, density is expected to influence the ability of males to find and monopolize mates, in turn, influencing variance in lifetime mating/reproductive success and the opportunity for selection. Herein, we investigate variance in male lifetime mating success (LMS), lifetime reproductive success (LRS), and the mating system of a sexually dimorphic carnivore that occurs at low densities, the polar bear (Ursus maritimus). Across 17 cohorts, born from 1975 to 1991, male LMS ranged from 0 to10 mates and LRS from 0 to 14 cubs; 40% of known-age males were not known to have reproduced. The opportunity for sexual selection (Is = 1.66, range = 0.60–4.99) and selection (I = 1.76, range: 0.65–4.89) were low compared to species with similar levels of sexual size dimorphism. Skew in male LRS was also low but significant for most cohorts indicating nonrandom reproductive success. Age-specific reproductive success was biased toward males from 11 to 17 years of age, with variation in fecundity (54%) but not longevity (10%) playing an important role in male reproduction. Our results support a growing body of evidence that suggests that male-biased size dimorphism and polygynous mating systems need not be associated with high variance in male mating and/or reproductive success.

Common Field Data Limitations Can Substantially Bias Sexual Selection Metrics.

Sexual selection studies widely estimate several metrics, but values may be inaccurate because standard field methods for studying wild populations produce limited data (e.g., incomplete sampling, inability to observe copulations directly). We compared four selection metrics (Bateman gradient, opportunity for sexual selection, opportunity for selection, and ) estimated with simulated complete and simulated limited data for 15 socially monogamous songbird species with extrapair paternity (4%-54% extrapair offspring). Inferring copulation success from offspring parentage creates nonindependence between these variables and systematically underestimates copulation success. We found that this introduces substantial bias for the Bateman gradient, opportunity for sexual selection, and . Notably, 47.5% of detected Bateman gradients were significantly positive for females, suggesting selection on females to copulate with multiple males, although the true Bateman gradient was zero. Bias generally increased with the extent of other sources of data limitations tested (nest predation, male infertility, and unsampled floater males). Incomplete offspring sampling introduced bias for all of the metrics except the Bateman gradient, while incomplete sampling of extrapair sires did not introduce additional bias when sires were a random subset of breeding males. Overall, our findings demonstrate how biases due to field data limitations can strongly impact the study of sexual selection.

Sexual Selection Does Not Increase the Rate of Compensatory Adaptation to a Mutation Influencing a Secondary Sexual Trait inDrosophila melanogaster

Theoretical work predicts that sexual selection can enhance natural selection, increasing the rate of adaptation to new environments and helping purge harmful mutations. While some experiments support these predictions, remarkably little work has addressed the role of sexual selection on compensatory adaptation—populations’ ability to compensate for the costs of deleterious alleles that are already present. We tested whether sexual selection, as well as the degree of standing genetic variation, affect the rate of compensatory evolution via phenotypic suppression in experimental populations of Drosophila melanogaster. These populations were fixed for a spontaneous mutation causing mild abnormalities in the male sex comb, a structure important for mating success. We fine-mapped this mutation to an ∼85 kb region on the X chromosome containing three candidate genes, showed that the mutation is deleterious, and that its phenotypic expression and penetrance vary by genetic background. We then performed experimental evolution, including a treatment where opportunity for mate choice was limited by experimentally enforced monogamy. Although evolved populations did show some phenotypic suppression of the morphological abnormalities in the sex comb, the amount of suppression did not depend on the opportunity for sexual selection. Sexual selection, therefore, may not always enhance natural selection; instead, the interaction between these two forces may depend on additional factors.

Seasonal variation in the allometry of wing pigmentation in adult males of the territorial damselfly Hetaerina vulnerata (Insecta Odonata)

Several sexually selected traits exhibit positive allometry. One of the explanations for this pattern suggests that positive allometry should be expected only for “pure” threat male signals, whilst isometry and negative allometry should occur in “pure” courtship signals. Wing pigmentation (WP) is a sexually selected trait exhibited by the males of several damselfly taxa (Odonata Zygoptera), which has been the focus of a number of studies of allometry. Whilst WP tends to exhibit positive allometry in many taxa, the pattern is not general. Previous studies have shown that in Hetaerina vulnerata, a territorial species in which WP is used as a “pure” threat signal, positive allometry is common. However, little attention has been paid to the seasonal variation in the allometry of WP in this species. To address this research gap, we collected data from a full reproductive season, from a natural population of H. vulnerata located in Central Mexico. Our results suggest that, first, male WP and body size generally increase throughout the season. Second, WP increases as the end of the season approaches, independently of body size. Finally, WP tends to be either not related to body size, or to exhibit isometry during the first half of the season (April–June), and positive allometry during the second half of the season (July–October). We suggest that our results may be explained by (i) the availability of resources critical to the development of larvae, as well as the duration of development, and (ii) an increase in the number or larger males towards the end of the season, which may favour the exaggeration of WP. Furthermore, the opportunity for sexual selection may vary, so that WP may be more relevant to male mating success towards the end of the reproductive season.

Environmental and demographic drivers of male mating success vary across sequential reproductive episodes in a polygynous breeder.

Ecological and social factors underpinning the inequality of male mating success in animal societies can be related to sex ratio, sexual conflict between breeders, effects of nonbreeders, resource dispersion, climatic conditions, and the various sequential stages of mating competition that constitute the sexual selection process. Here, we conducted an individual‐based study to investigate how local resource availability and demography interact with annual climate conditions to determine the degree of male mating inequality, and thus opportunity for sexual selection across two sequential reproductive episodes (harem and subsequent mate acquisition) in a naturally regulated (feral) horse population in Sable Island National Park Preserve, Canada. Using a 5‐year, spatially explicit, mark‐resight dataset and hierarchical mixed‐effects linear modeling, we evaluated the influence of adult sex ratio (ASR) on mating success and then tested for effects of freshwater availability, density, unpaired male abundance, and precipitation during each breeding season. Unpaired male abundance, freshwater availability, and ASR differed in their effects on male mating success according to year and selection episode. Opportunity for sexual selection in males associated with harem acquisition increased with ASR, and unpaired male abundance further explained weather‐related interannual variation after accounting for ASR. In contrast, once a harem was secured, ASR had little effect on male mating inequality in regard to acquiring additional females, while interannual variation in mating inequality increased with decreasing freshwater availability. Our findings show that local demography, resource availability, and weather effect opportunity for sexual selection in males differently depending on selection episode, and can attenuate or accentuate effects of ASR.

Mating System, Reproductive Success, and Sexual Selection in Bluntnose Klipfishes (Clinus cottoides).

A critical part of the sexual selection process in animals is the genetic mating system. Quantifying mating systems, especially in species with cryptic life histories can be challenging. One approach is to use genotypic markers and accurate parentage analysis, along with methods to account for bias when sampling natural populations, to calculate sexual selection metrics derived from Bateman's principles. In this study, 3 microsatellites were used to genotype 48 adults (23 female and 25 male) and 342 offspring from known mothers of live-bearing bluntnose klipfish. Parentage analysis was performed to interpret mating and reproductive success for both sexes. Metrics quantified were the opportunity for selection (I), the opportunity for sexual selection (Is), absolute (βss), and standardized (β'ss) Bateman gradients and the maximum intensity of precopulatory sexual selection (s'max). Multiple mating by both sexes were revealed by parentage analysis. However, females did not show significant Bateman gradients or a significant maximum intensity of precopulatory sexual selection (s'max), whereas male sexual selection metrics were all significantly greater than 0. These results suggest a polygynandrous mating system for this species. There is an opportunity for sexual selection to act on males but not females in this population, which is evolutionary tied to anisogamy, parental investment, and sex roles.

The opportunity for sexual selection and the evolution of non-responsiveness to pesticides, sterility inducers and contraceptives

We illustrate a method for delaying and possibly eliminating the evolution of non-responsiveness to the treatments now used to control pest populations. Using simulations and estimates of the variance in relative fitness, i.e., the opportunity for selection, in a rat-like mammal, we show that the selection responsible for the evolution of non-responsiveness to pesticides and sterility-inducers, is similar in its action to sexual selection, and for this reason can be orders of magnitude stronger than that which exists for untreated populations. In contrast, we show that when contraceptives are used to reduce the fertility of a pest species, with non-responders embedded within such populations, the opportunity for selection favoring non-responsiveness is reduced to that which is expected by chance alone. In pest species with separate sexes, we show that efforts to control pest populations or to mitigate selection favoring non-responsiveness, are likely to be ineffective when members of one sex are sterilized or killed. We also show that while mating preferences can impede the rate at which resistance evolves, they are more likely to accelerate this process, arguing against the use of sterile male approaches for controlling pests. Our results suggest that contraceptives are more effective at controlling pest populations and slowing the evolution of non-responsiveness than treatments that cause sterilization or death in target species. Furthermore, our results indicate that contraceptives that work differentially on each sex will be most effective in mitigating selection favoring non-responders. Our results have significant implications for the development and application of treatments to manage pests, now and into the future.

The effects of male harm vary with female quality and environmental complexity in Drosophila melanogaster.

Mate competition provides the opportunity for sexual selection which often acts strongly on males, but also the opportunity for sexual conflict that can alter natural selection on females. Recent attention has focused on the potential of sexual conflict to weaken selection on females if male sexual attention, and hence harm, is disproportionately directed towards high- over low-quality females, thereby reducing the fitness difference between these females. However, sexual conflict could instead strengthen selection on females if low-quality females are more sensitive to male harm than high-quality females, thereby magnifying fitness differences between them. We quantify the effects of male exposure on low- versus high-quality females in Drosophila melanogaster in each of two environments ('simple' and 'complex') that are known to alter behavioural interactions. We show that the effects of male harm are greater for low- compared to high-quality females in the complex but not the simple environment, consistent with mate competition strengthening selection on females in the former but not in the latter environment.

Refuge size variation and potential for sperm competition in Wellington tree weta.

Ecological variation in resources can influence the distribution and encounter rates of potential mates and competitors and, consequently, the opportunity for sexual selection. Factors that influence the likelihood that females mate multiply could also affect the potential for sperm competition. In Wellington tree weta (Hemideina crassidens, plural “weta”), the size of tree cavities (called galleries) used as refuges affects weta distribution and thus the opportunity for sexual selection and selection on male weaponry size. We examined the predicted effects of gallery size and male weaponry size on the potential for sperm competition. We asked if gallery size influenced the potential for multiple mating by females and potential for sperm competition, if male weaponry size was associated with relative expected sperm competition intensity (SCI), and if estimated male mating success was correlated with potential SCI. To quantify relative competitive environments of males, we created and analyzed networks of potential competitors based on which males could have mated with the same females. We found that small galleries had higher potential for female multiple mating and higher potential for sperm competition. Size of male weaponry was not associated with expected relative SCI. Regardless of gallery size, males with more potential mates were expected to face lower expected relative sperm competition. Thus, in this system, variation in the size of available refuges is likely to influence the potential for sperm competition, in a way that we might expect to increase variation in overall reproductive success.

Temporal patterns of extra-pair paternity in a population of Grasshopper Sparrows (Ammodramus savannarum) in Maryland

The incidence of extra-pair paternity (EPP) is highly variable across bird taxa. While EPP is known to affect reproductive variance, the causes of temporal variation in rates of EPP are poorly studied. Breeding density has often been proposed as an important factor influencing EPP variation, but it has received mixed support. Over a 5-year period we examined the rate of EPP in a socially monogamous Grasshopper Sparrow (Ammodramus savannarum) population on a restored grassland in Maryland. Of 124 broods, 62.1% had extra-pair young (EPY), and of 448 nestlings, 36.8% were the result of extra-pair fertilizations. Over the 5-year study, percent EPY ranged from 26% to 60%. EPP rates were positively correlated with the local density of territorial males, supporting the density hypothesis, and 81% of the EPY were from neighboring males. Male within-pair mating success was related to extra-pair mating, suggesting an active behavioral tradeoff between within- and extra-pair matings, especially at high densities. By examining males at the individual level, we found males that were not cuckolded also had the most genetic offspring (within-pair and extra-pair), whereas males that were cuckolded also failed to sire many extra-pair offspring. Here we show that density plays an important role in the availability of mates, EPP, and the opportunity for sexual selection. Received 9 April 2016. Accepted 3 August 2017.

Divergence in pollen performance between Clarkia sister species with contrasting mating systems supports predictions of sexual selection.

Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on postcopulatory male traits affecting siring success. In plants, closely related self- and cross-pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse-raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self-pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We tested for the effects of species, population, pollen type (self vs. outcross), the number of competing pollen grains, and temperature on pollen performance. Clarkia unguiculata exhibited higher mean PTGR than C. exilis; pollen type had no effect on performance in either taxon. The difference between these species in PTGR is consistent with predictions of sexual selection theory.