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.     

Transcriptome‐wide effects of sexual selection on the fate of new mutations

Sexual selection on males is predicted to have widespread effects on genetic variation as a consequence of the pleiotropic allelic effects on sexual and nonsexual traits. We manipulated the opportunity for sexual selection on males during 27 generations of mutation accumulation in inbred lines of Drosophila serrata, and used a microarray platform to investigate the effect of sexual selection on the expression of 2689 genes. While gene expression signal was, on average, higher in the absence of sexual selection, this difference was small (0.1%). In contrast, sexual selection impacted substantially on the mutational variance in gene expression. Over all genes, mutational variance in gene expression was, on average, 42% higher when sexual selection operated than when it was absent. Our results indicate that sexual selection on males can generate widespread effects across the genome. An increase in mutational variance without a corresponding change in mean suggested that most expression traits were unlikely to be under direct sexual selection. Instead, the mutational variance in gene expression traits is consistent with divergence generated by widespread pleiotropic associations with traits affecting male mating success.     

Sexual selection and its effect on the fixation of an asexual clone

Sexual selection is a powerful and ubiquitous force in sexual populations. It has recently been argued that sexual selection can eliminate the twofold cost of sex even with low genomic mutation rates. By means of differential male mating success, deleterious mutations in males become more deleterious than in females, and it has been shown that sexual selection can drastically reduce the mutational load in a sexual population, with or without any form of epistasis. However, any mechanism that claims to maintain sexual reproduction must be able to prevent the fixation of an asexual mutant clone with a twofold fitness advantage. Here, I show that despite very strong sexual selection, the fixation of an asexual mutant cannot be prevented under reasonable genomic mutation rates. Sexual selection can have a strong effect on the average mutational load in a sexual population, but as it cannot prevent the fixation of an asexual mutant, it is unlikely to play a key role on the maintenance of sexual reproduction.     

Mating behavior as an indicator of quality of Drosophila subobscura males?

According to current theoretical predictions, any deleterious mutations that reduce nonsexual fitness may have a negative influence on mating success. This means that sexual selection may remove deleterious mutations from the populations. Males of good genetic quality should be more successful in mating, compared to the males of lower genetic quality. As mating success is a condition dependent trait, large fractions of the genome may be a target of sexual selection and many behavioral traits are likely to be condition dependent. We manipulated the genetic quality of Drosophila subobscura males by inducing mutations with ionizing radiation and observed the effects of the obtained heterozygous mutations on male mating behavior: courtship occurrence, courtship latency, mating occurrence, latency to mating and duration of mating. We found possible effects of mutations. Females mated more frequently with male progeny of nonirradiated males and that these males courted females faster compared to the male progeny of irradiated males. Our findings indicate a possible important role of sexual selection in purging deleterious mutations.     

Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components

Two factors that can affect genetic load, synergistic epistasis and sexual selection, were investigated in Drosophila melanogaster. A set of five chromosomal regions containing visible recessive mutations were put together in all combinations to create a full set of 32 homozygous lines fixed for different numbers of known mutations. Two measures of fitness were made for each line: productivity (a combined measure of fecundity and egg-to-adult survivorship) and competitive male mating success. Productivity, but not male mating success, showed a pattern of strong average synergistic epistasis, such that the log fitness declined nonlinearly with increasing numbers of mutations. Synergistic epistasis is known to reduce the mutation load. Both fitness components show some positive and some negative interactions between specific sets of mutations. Furthermore, alleles with deleterious effects on productivity tend to also diminish male mating success. Given that male mating success can affect relative fitness without changing the mean productivity of a population, these additional effects would lead to lower frequencies and lower fixation rates of deleterious alleles without higher costs to the mean fitness of the population.     

Populations with elevated mutation load do not benefit from the operation of sexual selection

Theory predicts that if most mutations are deleterious to both overall fitness and condition-dependent traits affecting mating success, sexual selection will purge mutation load and increase nonsexual fitness. We explored this possibility with populations of mutagenized Drosophila melanogaster exhibiting elevated levels of deleterious variation and evolving in the presence or absence of male-male competition and female choice. After 60 generations of experimental evolution, monogamous populations exhibited higher total reproductive output than polygamous populations. Parental environment also affected fitness measures - flies that evolved in the presence of sexual conflict showed reduced nonsexual fitness when their parents experienced a polygamous environment, indicating trans-generational effects of male harassment and highlighting the importance of a common garden design. This cost of parental promiscuity was nearly absent in monogamous lines, providing evidence for the evolution of reduced sexual antagonism. There was no overall difference in egg-to-adult viability between selection regimes. If mutation load was reduced by the action of sexual selection in this experiment, the resultant gain in fitness was not sufficient to overcome the costs of sexual antagonism.     

PURGING THE GENOME WITH SEXUAL SELECTION: REDUCING MUTATION LOAD THROUGH SELECTION ON MALES

Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition‐dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females? In addition, the total effect of sexual selection on mutation load is complicated by possible increases in mutation rate that may be attributable to sexual selection. Finally, sexual selection affects population fitness not only through mutation load but also through sexual conflict, making it difficult to empirically measure how sexual selection affects load. Several lines of enquiry are suggested to better fill large gaps in our understanding of sexual selection and its effect on genetic load.     

Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation‐accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between‐sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between‐sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex‐limited, and/or sex‐biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual‐based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest‐to‐large fraction of mutations have sex‐limited (or highly sex‐biased) fitness effects, and (2) the average fitness effect of sex‐limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.     

MALE‐BIASED FITNESS EFFECTS OF SPONTANEOUS MUTATIONS IN DROSOPHILA MELANOGASTER

In populations with males and females, sexual selection may often represent a major component of overall selection. Sexual selection could act to eliminate deleterious alleles in concert with other forms of selection, thereby improving the fitness of sexual populations. Alternatively, the divergent reproductive strategies of the sexes could promote the maintenance of sexually antagonistic variation, causing sexual populations to be less fit. The net impact of sexual selection on fitness is not well understood, due in part to limited data on the sex‐specific effects of spontaneous mutations on total fitness. Using a set of mutation accumulation lines of Drosophila melanogaster, we found that mutations were deleterious in both sexes and had larger effects on fitness in males than in females. This pattern is expected to reduce the mutation load of sexual females and promote the maintenance of sexual reproduction.     

Eutrophication and predation risk interact to affect sexual trait expression and mating success

Sexual traits are especially sensitive to low food resources. Other environmental parameters (e.g., predation) should also affect sexual trait expression by favoring investment in viability traits rather than sexual traits. We know surprisingly little about how predators alter investment in sexual traits, or how predator and resource environments interact to affect sexual trait investment. We explored how increasing phosphorous (P) availability, at a level mimicking cultural eutrophication, affects the development of sexual, nonsexual, and viability traits of amphipods in the presence and absence of predators. Sexual traits and growth were hypersensitive to low P compared to nonsexual traits. However, a key sexual trait responded to low P only when predator cues were absent. Furthermore, investment trade-offs between sexual traits and growth only occurred when P was low. The phenotypic changes caused by predator cues and increased P availability resulted in higher male mating success. Thus, eutrophication not only affects sexual trait expression but also masks the trade-off between traits with similar P demand. Sensitivity of sexually selected traits to changes in P, combined with the important roles these traits play in determining fitness and driving speciation, suggests that human-induced environmental change can greatly alter the evolutionary trajectories of populations.     

Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster

The effects of sexual selection on population mean fitness are unclear and a subject of debate. Recent models propose that, because reproductive success may be condition dependent, much of the genome may be a target of sexual selection. Under this scenario, mutations that reduce health, and thus nonsexual fitness, may also be deleterious with respect to reproductive success, meaning that sexual selection may contribute to the purging of deleterious alleles. We tested this hypothesis directly by subjecting replicate Drosophila melanogaster populations to two treatments that altered the opportunity for sexual selection and then tracked changes in the frequency of six separate deleterious alleles with recessive and visible phenotypic effects. While natural selection acted to decrease the frequency of all six mutations, the addition of sexual selection did not aid in the purging of any of them, and for three of them appears to have hampered it. Courtship and mating have harmful effects in this species and mate choice assays showed that males directed more courtship and mating behavior toward wild-type over mutant females, providing a likely explanation for sexual selection's cost. Whether this cost extends to other mutations (e.g., those lacking visible phenotypic effects) is an important topic for future research.     

Inbreeding depression in the competitive fertilization success of male crickets

Mating between close relatives generally results in offspring of decreased fitness. Inbreeding depression is generally greater for life-history traits than for morphological traits, and recent studies of traits subject to sexual selection suggest that these may suffer the greatest inbreeding depression. Sexual selection continues after mating in the form of sperm competition and cryptic female choice, imposing strong selection on male competitive fertilization success. Here, I examine the effects of a single generation of full-sib mating on competitive fertilization success in a cricket, Teleogryllus oceanicus. The estimated coefficient of inbreeding depression in competitive fertilization success was 0.37, higher than that for other life-history and morphological traits. Such intense inbreeding depression coupled with little or no additive genetic variance for this trait is consistent with strong directional selection on male competitive fertilization success generating high levels of dominance variance, and provides an adaptive explanation for the evolution of inbreeding avoidance found in this species.     

Testing the prediction from sexual selection of a positive genetic correlation between human mate preferences and corresponding traits

Sexual selection can cause evolution in traits that affect mating success, and it has thus been implicated in the evolution of human physical and behavioural traits that influence attractiveness. We use a large sample of identical and nonidentical female twins to test the prediction from mate choice models that a trait under sexual selection will be positively genetically correlated with preference for that trait. Six of the eight preferences we investigated, i.e. height, hair colour, intelligence, creativity, exciting personality, and religiosity, exhibited significant positive genetic correlations with the corresponding traits, while the personality measures ‘easy going’ and ‘kind and understanding’ exhibited no phenotypic or genetic correlation between preference and trait. The positive results provide important evidence consistent with the involvement of sexual selection in the evolution of these human traits.     

The effects of sexual selection on life‐history traits: an experimental study on guppies

Sexual selection is often prevented during captive breeding in order to maximize effective population size and retain genetic diversity. However, enforcing monogamy and thereby preventing sexual selection may affect population fitness either negatively by preventing the purging of deleterious mutations or positively by reducing sexual conflicts. To better understand the effect of sexual selection on the fitness of small populations, we compared components of female fitness and the expression of male secondary sexual characters in 19 experimental populations of guppies (Poecilia reticulata) maintained under polygamous or monogamous mating regimes over nine generations. In order to generate treatments that solely differed by their level of sexual selection, the middle‐class neighbourhood breeding design was enforced in the monogamous populations, while in the polygamous populations, all females contributed similarly to the next generation with one male and one female offspring. This experimental design allowed potential sexual conflicts to increase in the polygamous populations because selection could not operate on adult‐female traits. Clutch size and offspring survival showed a weak decline from generation to generation but did not differ among treatments. Offspring size, however, declined across generations, but more in monogamous than polygamous populations. By generation eight, orange‐ and black‐spot areas were larger in males from the polygamous treatment, but these differences were not statistically significant. Overall, these results suggest that neither sexual conflict nor the purging of deleterious mutation had important effects on the fitness of our experimental populations. However, only few generations of enforced monogamy in a benign environment were sufficient to negatively affect offspring size, a trait potentially crucial for survival in the wild. Sexual selection may therefore, under certain circumstances, be beneficial over enforced monogamy during captive breeding.     

The mutational structure of metabolism in Caenorhabditis elegans

A properly functioning organism must maintain metabolic homeostasis. Deleterious mutations degrade organismal function, presumably at least in part via effects on metabolic function. Here we present an initial investigation into the mutational structure of the Caenorhabditis elegans metabolome by means of a mutation accumulation experiment. We find that pool sizes of 29 metabolites vary greatly in their vulnerability to mutation, both in terms of the rate of accumulation of genetic variance (the mutational variance, VM) and the rate of change of the trait mean (the mutational bias, ΔM). Strikingly, some metabolites are much more vulnerable to mutation than any other trait previously studied in the same way. Although we cannot statistically assess the strength of mutational correlations between individual metabolites, principal component analysis provides strong evidence that some metabolite pools are genetically correlated, but also that there is substantial scope for independent evolution of different groups of metabolites. Averaged over mutation accumulation lines, PC3 is positively correlated with relative fitness, but a model in which metabolites are uncorrelated with fitness is nearly as good by Akaike's Information Criterion.     

Nonlinear effects of female mate choice in wild threespine sticklebacks

Sexual selection by mate choice represents a very important selective pressure in many animal species and might have evolutionary impacts beyond exaggeration of secondary sexual traits. Describing the shape and strength of the relationships linking mating success and nonsexual traits in natural conditions represents a challenging step in our understanding of adaptive evolution. We studied the effect of behavioral (nest site choice), immunological (trematode level of infection), genetic diversity (measured by mean d2) and morphological (standard length and pectoral fin size) traits on male mating success in a natural population of threespine sticklebacks Gasterosteaus aculeatus. Male mating success was measured by microsatellite genotyping of embryos used to infer female genotypes. First, we analyzed all territorial males (full analysis) but also considered independently only males with a nonzero mating success (reduced analysis) because some of the males with no eggs could have been part of a later breeding cycle. Multiple linear regressions identified a significant negative effect of parasite load in the full analysis, whereas no linear effect was found in the reduced analysis. The quadratic analyses revealed that nest location and parasite load were significantly related to mating success by positive (concave selection) and negative (convex selection) quadratic coefficients respectively, resulting in a saddle-shaped fitness surface. Moreover, there were significant interactions between nest location, mean d2 and parasite load in the reduced analysis. The subsequent canonical rotation of the matrix of quadratic and cross-product terms identified two major axes of the response surface: a vector representing mostly nest site choice and a vector representing parasite load. These results imply that there exists more than one way for a male threespine stickleback to maximize its mating success and that such nonlinear relationships between male mating success induced by female mate choice and male characteristics might have been overlooked in many studies.     

Assessing the alignment of sexual and natural selection using radiomutagenized seed beetles

A major unsolved question in evolutionary biology concerns the relationship between natural and sexual selection. Sexual selection might augment natural selection, for example if mutations that harm female fecundity also reduce male mating success. Conversely, sexual selection might favour traits that impair naturally selected fitness components. We induced detrimental mutations in Callosobruchus maculatus beetles using X‐ray irradiation and then experimentally measured the effect of precopulatory sexual selection on offspring number and survival rate. Sexual selection treatment had a negative effect on egg‐to‐adult survivorship, although the number of progeny reaching adulthood was unaffected, perhaps because eggs and juveniles that failed to develop lessened competition on the survivors. We hypothesize that the negative effect of sexual selection arose because sexually competitive males transmitted a smaller nuptial gift or carried alleles that conferred reduced survival. Although we found no evidence that sexual selection on males can purge alleles that are detrimental to naturally selected fitness components, such benefits might exist in other environmental or genetic contexts.     

A test for epistasis among induced mutations in Caenorhabditis elegans

Synergistic epistasis, in which deleterious mutations tend to magnify each other's effects, is a necessary component of the mutational deterministic hypothesis for the maintenance of sexual production. We tested for epistasis for life-history traits in the soil nematode Caenorhabditis elegans by inducing mutations in two genetic backgrounds: a wild-type strain and a set of genetically loaded lines that contain large numbers of independent mildly detrimental mutations. There was no significant difference between the effect of new mutations on the wild-type background and the genetically loaded background for four out of five fitness correlates. In these four cases, the maximum level of epistasis compatible with the data was very low. The fifth trait, late productivity, is not likely to be an important component of fitness. This suggests either that specific environmental conditions are required to cause epistasis or that synergistic epistasis is not a general phenomenon. We also suggest a new mechanism by which deleterious mutations may provide an advantage to sexual reproduction under low selection coefficients.     

Dietary stress does not strengthen selection against single deleterious mutations in Drosophila melanogaster

Stress is generally thought to increase the strength of selection, although empirical results are mixed and general conclusions are difficult because data are limited. Here we compare the fitness effects of nine independent recessive mutations in Drosophila melanogaster in a high- and low-dietary-stress environment, estimating the strength of selection on these mutations arising from both a competitive measure of male reproductive success and productivity (female fecundity and the subsequent survival to adulthood of her offspring). The effect of stress on male reproductive success has not been addressed previously for individual loci and is of particular interest with respect to the alignment of natural and sexual selection. Our results do not support the hypothesis that stress increases the efficacy of selection arising from either fitness component. Results concerning the alignment of natural and sexual selection were mixed, although data are limited. In the low-stress environment, selection on mating success and productivity were concordant for five of nine mutations (four out of four when restricted to those with significant or near-significant productivity effects), whereas in the high-stress environment, selection aligned for seven of nine mutations (two out of two when restricted to those having significant productivity effects). General conclusions as to the effects of stress on the strength of selection and the alignment of natural and sexual selection await data from additional mutations, fitness components and stressors.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.