Variance In Male Mating Success Research Articles

Phylogenomics of the extinct Heath Hen provides support for sex-biased introgression among extant prairie grouse

Rapid divergence and subsequent reoccurring patterns of gene flow can complicate our ability to discern phylogenetic relationships among closely related species. To what degree such patterns may differ across the genome can provide an opportunity to extrapolate better how life history constraints may influence species boundaries. By exploring differences between autosomal and Z (or X) chromosomal-derived phylogenetic patterns, we can better identify factors that may limit introgression despite patterns of incomplete lineage sorting among closely related taxa. Here, using a whole-genome resequencing approach coupled with an exhaustive sampling of subspecies within the recently divergent prairie grouse complex (genus: Tympanuchus), including the extinct Heath Hen (T. cupido cupido), we show that their phylogenomic history differs depending on autosomal or Z-chromosome partitioned SNPs. Because the Heath Hen was allopatric relative to the other prairie grouse taxa, its phylogenetic signature should not be influenced by gene flow. In contrast, all the other extant prairie grouse taxa, except Attwater’s Prairie-chicken (T. c. attwateri), possess overlapping contemporary geographic distributions and have been known to hybridize. After excluding samples that were likely translocated prairie grouse from the Midwest to the eastern coastal states or their resulting hybrids with mainland Heath Hens, species tree analyses based on autosomal SNPs consistently identified a paraphyletic relationship with regard to the Heath Hen with Lesser Prairie-chicken (T. pallidicinctus) sister to Greater Prairie-chicken (T. c. pinnatus) regardless of genic or intergenic partitions. In contrast, species trees based on the Z-chromosome were consistent with Heath Hen sister to a clade that included its conspecifics, Greater and Attwater’s Prairie-chickens (T. c. attwateri). These results were further explained by historic gene flow, as shown with an excess of autosomal SNPs shared between Lesser and Greater Prairie-chickens but not with the Z-chromosome. Phylogenetic placement of Sharp-tailed Grouse (T. phasianellus), however, did not differ among analyses and was sister to a clade that included all other prairie grouse despite low levels of autosomal gene flow with Greater Prairie-chicken. These results, along with strong sexual selection (i.e., male hybrid behavioral isolation) and a lek breeding system (i.e., high variance in male mating success), are consistent with a pattern of female-biased introgression between prairie grouse taxa with overlapping geographic distributions. Additional study is warranted to explore how genomic components associated with the Z-chromosome influence the phenotype and thereby impact species limits among prairie grouse taxa despite ongoing contemporary gene flow.

Sexual selection in seaweed? Testing Bateman's principles in the red alga Gracilaria gracilis.

In anisogamous species, sexual selection is expected to be stronger in males. Bateman's principles state that the variance in (i) reproductive and (ii) mating success is greater for males, and (iii) the relationship between reproductive success and mating success (the Bateman gradient) is also stronger for males than for females. Sexual selection, based on Bateman's principles, has been demonstrated in animals and some angiosperms, but never in a seaweed. Here we focus on the oogamous haploid-diploid rhodophyte Gracilaria gracilis in which previous studies have shown evidence for non-random mating, suggesting the existence of male-male competition and female choice. We estimated mating and reproductive success using paternity analyses in a natural population where up to 92% of fertilizations occurred between partners of that population. The results show that the variance in mating success is significantly greater in males than in females and that the Bateman gradient is positive only in males. Distance to female partners also explains a minor part of the variance in male mating success. Although there is no evidence for sexual dimorphism, our study supports the hypothesis that sexual selection occurs in G. gracilis, probably on male traits, even if we cannot observe, characterize or quantify them yet.

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load.

Sexual selection on males is predicted to increase population fitness, and delay population extinction, when mating success negatively covaries with genetic load across individuals. However, such benefits of sexual selection could be counteracted by simultaneous increases in genome-wide drift resulting from reduced effective population size caused by increased variance in fitness. Resulting fixation of deleterious mutations could be greatest in small populations, and when environmental variation in mating traits partially decouples sexual selection from underlying genetic variation. The net consequences of sexual selection for genetic load and population persistence are therefore likely to be context dependent, but such variation has not been examined. We use a genetically explicit individual-based model to show that weak sexual selection can increase population persistence time compared to random mating. However, for stronger sexual selection such positive effects can be overturned by the detrimental effects of increased genome-wide drift. Furthermore, the relative strengths of mutation-purging and drift critically depend on the environmental variance in the male mating trait. Specifically, increasing environmental variance caused stronger sexual selection to elevate deleterious mutation fixation rate and mean selection coefficient, driving rapid accumulation of drift load and decreasing population persistence times. These results highlight an intricate balance between conflicting positive and negative consequences of sexual selection on genetic load, even in the absence of sexually antagonistic selection. They imply that environmental variances in key mating traits, and intrinsic genetic drift, should be properly factored into future theoretical and empirical studies of the evolution of population fitness under sexual selection.

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success.

Many studies ask whether young or older males are better at acquiring mates. Even so, how age affects reproductive success is still poorly understood because male age and mating history are confounded in most studies: older males usually have more mating experience. To what extent does mating history rather than age explain variation in male mating success? And how do mating history and male age determine paternity when there is also postcopulatory sexual selection? Here, we experimentally manipulated the mating history of old and young males in the eastern mosquitofish (Gambusia holbrooki). We then recorded male mating behavior and share of paternity (1259 offspring from 232 potential sires) when they competed for mates and fertilizations. Old males, and males with no mating experience, spent significantly more time approaching females, and attempting to mate, than did young males and those with greater mating experience. Male age and mating history interacted to affect paternity: old males benefited from having previous mating experience, but young males did not. Our results highlight that the age-related changes in male reproductive traits and in paternity that have been described in many taxa may be partly attributable to male mating history and not simply to age itself.

Mating has opposite effects on male and female sexually selected cuticular hydrocarbons

In Drosophila serrata flies, there is female choice for male cuticular hydrocarbon (CHC) profiles and male choice for female CHC profiles. Furthermore, both males and females can alter their CHCs: when there is more opportunity for mating, males express combinations of CHCs preferred by females; however, females appear to change CHC profiles to avoid male harassment. In this study, I investigate the effect of number of matings (0–4) on male and female sexually selected CHCs. Mating caused males to express CHCs associated with higher male mating success. Thus, successfully mating males are likely to have increased future mating success. Conversely, females that mated more times expressed CHC profiles that were associated with lower female mating success. Females maximized their offspring production by mating more than once, but additional matings did not provide additional benefits. Furthermore, number of matings did not affect female survival. In total, these results suggest that females alter CHC expression to discourage male courtship when additional matings are not beneficial. In conclusion, plasticity in male and female CHC expression can both increase variance in male mating success and decrease variance in female mating success, driving the evolution of sexually selected chemical signals.

Sperm competition, but not major histocompatibility divergence, drives differential fertilization success between alternative reproductive tactics in Chinook salmon

Post-copulatory sexual selection processes, including sperm competition and cryptic female choice (CFC), can operate based on major histocompatibility (MH) genes. We investigated sperm competition between male alternative reproductive tactics [jack (sneaker) and hooknose (guard)] of Chinook salmon (Oncorhynchus tshawytscha). Using a full factorial design, we examined invitro competitive fertilization success of paired jack and hooknose males at three time points after sperm activation (0, 15 and 60s) to test for male competition, CFC and time effects on male fertilization success. We also examined egg-mediated CFC at two MH genes by examining both the relationship between competitive fertilization success and MH divergence as well as inheritance patterns of MH alleles in resulting offspring. We found that jacks sired more offspring than hooknose males at 0s post-activation; however, jack fertilization success declined over time post-activation, suggesting a trade-off between sperm speed and longevity. Enhanced fertilization success of jacks (presumably via higher sperm quality) may serve to increase sneaker tactic competitiveness relative to dominant hooknose males. We also found evidence of egg-mediated CFC (i.e. female×male interaction) influencing competitive fertilization success; however, CFC was not acting on the MH genes as we found no relationship between fertilization success and MH II β1 or MH I α1 divergence and we found no deviations from Mendelian inheritance of MH alleles in the offspring. Our study provides insight into evolutionary mechanisms influencing variation in male mating success within alternative reproductive tactics, thus underscoring different strategies that males can adopt to attain success.

Do males with higher mating success invest more in armaments? An across‐populations study in damselflies

1. Males with higher mating success would be expected to invest more in traits that facilitate mating, leading to steeper allometry of those traits with respect to body size. Across‐population studies following latitudinal variation in male mating success are an excellent study system to address this question.2. Males of the damselfly Lestes sponsa were used to investigate whether the allometric patterns of the length and width of the anal appendages, used for grasping the female prior to mating, corresponded to male mating success. Across a large latitudinal gradient, it was hypothesised that there is a larger investment in the grasping apparatus, i.e. a steeper allometric slope, following higher mating success.3. Behavioural observations in field enclosures showed the highest mating success at high latitude, while there were no significant differences in mating success between the central and low latitudes. Positive allometry was found for the length of the anal appendages in high‐latitude males, while central‐ and low‐latitude males showed no significant regressions of the traits on body size.4. These results partially support the hypothesis, as high‐latitude, more successful males invested more in the length (but not the width) of the grasping apparatus than did central‐ and low‐latitude males. Therefore, higher mating success might be facilitated by larger investment in armaments. Intraspecific studies on allometric patterns of traits that participate in mating success might offer new insights into the role of those traits in the reproductive behaviour of a species.

Artificial selection on mating competitiveness of Anastrepha ludens for sterile insect technique application

AbstractThe sterile insect technique (SIT) has been applied successfully for the control of several fruit fly species of economic importance. In species with lek mating systems, as in the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae) – where the variance in male mating success is high, males have to compete with other males, and where wild females are highly selective – the success of SIT depends on the sexual competitiveness of mass‐reared sterile males. However, mass‐rearing conditions result in selection of sexual behavioral traits that differ from wild flies, reducing mating competitiveness of sterile flies and SIT efficiency. Artificial selection in mass‐rearing colonies, based on male mating success, represents an alternative to improve the sexual performance of sterile males. Here, we evaluated the effect of selection of A. ludens mass‐reared males based on their mating competitiveness. Two modes of selection were compared, one single selection event on parental flies, and continuous selection along four consecutive generations. For the offspring of each treatment in each generation, we evaluated male mating success, its association with post‐copulatory behavior through female remating inhibition, and life‐history traits that are key for mass‐rearing, such as immature survival and reproduction. Field cage mating tests revealed that wild males were more competitive than mass‐reared males (selected and unselected). Although no significant differences were found between mass‐reared selected and non‐selected males, in the fourth generation males from the selected colonies performed better than males from the non‐selected colonies and their mating competitiveness was similar to that of wild males. No consistent differences were observed in mating latency, copulation duration, or ability to inhibit female remating. Survival and fecundity decreased with increasing rearing generations, except in the colony with continuous selection where fecundity and fertility increased.

Ecological and Social Factors Constrain Spatial and Temporal Opportunities for Mating in a Migratory Songbird.

Many studies of sexual selection assume that individuals have equal mating opportunities and that differences in mating success result from variation in sexual traits. However, the inability of sexual traits to explain variation in male mating success suggests that other factors moderate the strength of sexual selection. Extrapair paternity is common in vertebrates and can contribute to variation in mating success and thus serves as a model for understanding the operation of sexual selection. We developed a spatially explicit, multifactor model of all possible female-male pairings to test the hypothesis that ecological (food availability) and social (breeding density, breeding distance, and the social mate's nest stage) factors influence an individual's opportunity for extrapair paternity in a socially monogamous bird, the black-throated blue warbler, Setophaga caerulescens. A male's probability of siring extrapair young decreased with increasing distance to females, breeding density, and food availability. Males on food-poor territories were more likely to sire extrapair young, and these offspring were produced farther from the male's territory relative to males on food-abundant territories. Moreover, males sired extrapair young mostly during their social mates' incubation stage, especially males on food-abundant territories. This study demonstrates how ecological and social conditions constrain the spatial and temporal opportunities for extrapair paternity that affect variation in mating success and the strength of sexual selection in socially monogamous species.

Correlational selection on personality and social plasticity: morphology and social context determine behavioural effects on mating success.

Despite a central line of research aimed at quantifying relationships between mating success and sexually dimorphic traits (e.g., ornaments), individual variation in sexually selected traits often explains only a modest portion of the variation in mating success. Another line of research suggests that a significant portion of the variation in mating success observed in animal populations could be explained by correlational selection, where the fitness advantage of a given trait depends on other components of an individual's phenotype and/or its environment. We tested the hypothesis that interactions between multiple traits within an individual (phenotype dependence) or between an individual's phenotype and its social environment (context dependence) can select for individual differences in behaviour (i.e., personality) and social plasticity. To quantify the importance of phenotype- and context-dependent selection on mating success, we repeatedly measured the behaviour, social environment and mating success of about 300 male stream water striders, Aquarius remigis. Rather than explaining individual differences in long-term mating success, we instead quantified how the combination of a male's phenotype interacted with the immediate social context to explain variation in hour-by-hour mating decisions. We suggest that this analysis captures more of the mechanisms leading to differences in mating success. Males differed consistently in activity, aggressiveness and social plasticity. The mating advantage of these behavioural traits depended on male morphology and varied with the number of rival males in the pool, suggesting mechanisms selecting for consistent differences in behaviour and social plasticity. Accounting for phenotype and context dependence improved the amount of variation in male mating success we explained statistically by 30-274%. Our analysis of the determinants of male mating success provides important insights into the evolutionary forces that shape phenotypic variation. In particular, our results suggest that sexual selection is likely to favour individual differences in behaviour, social plasticity (i.e., individuals adjusting their behaviour), niche preference (i.e., individuals dispersing to particular social conditions) or social niche construction (i.e., individuals modifying the social environment). The true effect of sexual traits can only be understood in interaction with the individual's phenotype and environment.

Trade-Offs in Male Display Activity with Lek Size.

In lek mating systems, males aggregate and defend arenas where they display for females; females select and mate with a male and then solely raise their offspring. Generally, female visits and copulations increase and reproductive variance in male mating success declines with lek size. Here we investigate how male display effort changes across a gradient in lek size. We expect male display effort, an energetically expensive activity, will increase with lek size and male rank due to changes in breeding opportunities and competition among males. We test the interaction of male rank and lek size on display effort using the white-bearded manakin, Manacus manacus (Aves: Pipridae), a well-studied species with a wide geographic distribution in the new world tropics. We used mini-video recorders to simultaneously capture female visits and display behaviors of 41 males distributed over 10 leks. We found that overall display effort increased disproportionately with lek size due to males of both high and low ranks increasing their display effort at larger leks. Our results suggest that increased breeding opportunities and intrasexual competition at larger leks result in males of different ranks investing similarly in increased display effort in order to attract females.

Low reproductive skew despite high male-biased operational sex ratio in a glass frog with paternal care.

BackgroundReproductive skew, the uneven distribution of reproductive success among individuals, is a common feature of many animal populations. Several scenarios have been proposed to favour either high or low levels of reproductive skew. Particularly a male-biased operational sex ratio and the asynchronous arrival of females is expected to cause high variation in reproductive success among males. Recently it has been suggested that the type of benefits provided by males (fixed vs. dilutable) could also strongly impact individual mating patterns, and thereby affecting reproductive skew. We tested this hypothesis in Hyalinobatrachium valerioi, a Neotropical glass frog with prolonged breeding and paternal care.ResultsWe monitored and genetically sampled a natural population in southwestern Costa Rica during the breeding season in 2012 and performed parentage analysis of adult frogs and tadpoles to investigate individual mating frequencies, possible mating preferences, and estimate reproductive skew in males and females. We identified a polygamous mating system, where high proportions of males (69 %) and females (94 %) reproduced successfully. The variance in male mating success could largely be attributed to differences in time spent calling at the reproductive site, but not to body size or relatedness. Female H. valerioi were not choosy and mated indiscriminately with available males.ConclusionsOur findings support the hypothesis that dilutable male benefits - such as parental care - can favour female polyandry and maintain low levels of reproductive skew among males within a population, even in the presence of direct male-male competition and a highly male-biased operational sex ratio. We hypothesize that low male reproductive skew might be a general characteristic in prolonged breeders with paternal care.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0469-z) contains supplementary material, which is available to authorized users.

Environment-Dependent Sexual Selection: Bateman's Parameters under Varying Levels of Food Availability.

Sexual selection is a potent evolutionary force that has been shown to vary in strength and direction depending on demographic factors such as density and sex ratio. However, the effect of other environmental factors on the mode of sexual selection remains largely unexplored. Here, we tested experimentally how food restriction affects the potential for sexual selection in the male and the female sex function of the simultaneously hermaphroditic freshwater snail Physa acuta. We manipulated food availability and compared Bateman's metrics of sexual selection between groups of five well-fed and five food-restricted snails. Food-restricted individuals had a reduced female reproductive output, suggesting that we successfully manipulated the reproductive resources. Importantly, food restriction reduced the male opportunity for sexual selection (in terms of a lowered variance in male mating success) and led to diminishing returns of mating in both sexes (in terms of nonsignificant Bateman gradients). Furthermore, we observed significant changes in the relative contribution of different fitness components, suggesting stronger postcopulatory selection in the male sex role and stronger fecundity selection in the female sex role under restricted food conditions. This study highlights the need to incorporate ecological factors to better understand how sexual selection operates in the wild.

Experimental food supplementation reveals habitat-dependent male reproductive investment in a migratory bird.

Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability-one key aspect of habitat quality-on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.

Variation in promiscuity and sexual selection drives avian rate of Faster-Z evolution.

Higher rates of coding sequence evolution have been observed on the Z chromosome relative to the autosomes across a wide range of species. However, despite a considerable body of theory, we lack empirical evidence explaining variation in the strength of the Faster‐Z Effect. To assess the magnitude and drivers of Faster‐Z Evolution, we assembled six de novo transcriptomes, spanning 90 million years of avian evolution. Our analysis combines expression, sequence and polymorphism data with measures of sperm competition and promiscuity. In doing so, we present the first empirical evidence demonstrating the positive relationship between Faster‐Z Effect and measures of promiscuity, and therefore variance in male mating success. Our results from multiple lines of evidence indicate that selection is less effective on the Z chromosome, particularly in promiscuous species, and that Faster‐Z Evolution in birds is due primarily to genetic drift. Our results reveal the power of mating system and sexual selection in shaping broad patterns in genome evolution.

Territory defense as a condition-dependent component of male reproductive success in Drosophila serrata.

Sexual selection arises from both intrasexual competition and mate choice. With respect to the evolution of male traits, there is a vast literature documenting the existence of female choice and male-male competition, and both have been shown to co-occur in many species. Despite numerous studies of these two components of male reproductive success in isolation, few have investigated whether and how they interact to determine total sexual selection. To address this, we investigate male territoriality in Drosophila serrata, a species in which female preference for male sexual pheromones (cuticular hydrocarbons or CHCs) have been extensively studied. We demonstrate that territoriality occurs, that it involves direct male-male aggressive interactions, and that it contributes to variation in male mating success. Results from a phenotypic manipulation also indicate that territorial success is condition-dependent, although a genetic manipulation of condition, involving three generations of full-sib inbreeding, failed to find a significant effect. Finally, selection assays also suggest that territorial success depends on male body size but not on CHCs, whereas the opposite is true for mating success.

Limited indirect fitness benefits of male group membership in a lekking species.

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group-level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.

Sexual Selection, Epistasis and Species Boundaries in Sympatric Hawaiian Picture-winged Drosophila

The Hawaiian picture-winged flies in the genus Drosophila are a spectacular example of rapid evolutionary diversification in which sexual selection is considered an important mechanism for reproductive isolation and speciation. We investigated the behavioral reproductive isolation of two closely related and sympatric Hawaiian picture-winged Drosophila species, D. silvestris and D. heteroneura, which are known to hybridize in nature and produce viable and fertile hybrids. We compared the mating success of parental, F1 and backcross males in pairings with D. heteroneura females. The F1 males were produced by mating D. heteroneura males with D. silvestris females, and the backcross males were produced by mating F1 females with D. heteroneura males. The mating success of backcross males paired with D. heteroneura females were significantly reduced relative to that of parental and F1 males. This reduced mating success occurred primarily at a late stage of courtship where female choice of mate may be important. Two- and three-gene models demonstrate that epistasis involving a few genes could account for the observed variation in male mating success. These results are consistent with negative epistasis in the backcross generation and support the importance of sexual selection and negative epistasis in the evolution and maintenance of these species.

Sexual selection and the differential effect of polyandry.

In principle, widespread polyandry (female promiscuity) creates potential for sexual selection in males both before and after copulation. However, the way polyandry affects pre- and postcopulatory episodes of sexual selection remains little understood. Resolving this fundamental question has been difficult because it requires extensive information on mating behavior as well as paternity for the whole male population. Here we show that in replicate seminatural groups of red junglefowl, Gallus gallus, polyandry eroded variance in male mating success, which simultaneously weakened the overall intensity of sexual selection but increased the relative strength of postcopulatory episodes. We further illustrate the differential effect of polyandry on pre- and postcopulatory sexual selection by considering the case of male social status, a key determinant of male reproductive success in this species. In low-polyandry groups, however, status was strongly sexually selected before copulation because dominants mated with more females. In high-polyandry groups, sexual selection for status was weakened and largely restricted after copulation because dominants defended paternity by mating repeatedly with the same female. These results reveal polyandry as a potent and dynamic modulator of sexual selection episodes.

Turtle mating patterns buffer against disruptive effects of climate change.

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.