Fathers and sons, mothers and daughters: Sex-specific genetic architecture for fetal testosterone in a wild mammal.

Testosterone plays a critical role in mediating fitness-related traits in many species. Although it is highly responsive to environmental and social conditions, evidence from several species show a heritable component to its individual variation. Despite the known effects that in utero testosterone exposure have on adult fitness, the heritable component of individual testosterone variation in fetuses is mostly unexplored. Furthermore, testosterone has sex-differential effects on fetal development, i.e., a specific level may be beneficial for male fetuses but detrimental for females, producing sexual conflict. Such sexual conflict may be resolved by the evolution of a sex-specific genetic architecture of the trait. Here, we quantified fetal testosterone levels in a wild species, free-ranging nutrias (Myocastor coypus) using hair-testing and estimated testosterone heritability between parent and offspring from the same and opposite sex. We found that in utero accumulated hair testosterone levels were heritable between parents and offspring of the same sex. Moreover, there was a low additive genetic covariance between the sexes, and a low cross-sex genetic correlation, suggesting a potential for sex-specific trait evolution, expressed early on, in utero.

Evolutionary rescue from climate change: male indirect genetic effects on lay-dates and their consequences for population persistence.

Changes in avian breeding phenology are among the most apparent responses to climate change in free-ranging populations. A key question is whether populations will be able to keep up with the expected rates of environmental change. There is a large body of research on the mechanisms by which avian lay-dates track temperature change and the consequences of (mal)adaptation on population persistence. Often overlooked is the role of males, which can influence the lay-date of their mate through their effect on the prelaying environment. We explore how social plasticity causing male indirect genetic effects can help or hinder population persistence when female genes underpinning lay-date and male genes influencing female's timing of reproduction both respond to climate-mediated selection. We extend quantitative genetic moving optimum models to predict the consequences of social plasticity on the maximum sustainable rate of temperature change, and evaluate our model using a combination of simulated data and empirical estimates from the literature. Our results suggest that predictions for population persistence may be biased if indirect genetic effects and cross-sex genetic correlations are not considered and that the extent of this bias depends on sex differences in how environmental change affects the optimal timing of reproduction. Our model highlights that more empirical work is needed to understand sex-specific effects of environmental change on phenology and the fitness consequences for population dynamics. While we discuss our results exclusively in the context of avian breeding phenology, the approach we take here can be generalized to many different contexts and types of social interaction.

Adult body mass is heritable, positively genetically correlated and under selection of differing shapes between the sexes in a bird with little apparent sexual dimorphism.

In most animals, body mass varies with ecological conditions and is expected to reflect how much energy can be allocated to reproduction and survival. Because the sexes often differ in their resource acquisition and allocation strategies, variations in adult body mass and their consequences on fitness can differ between the sexes. Assessing the relative contributions of environmental and genetic effects (i.e. heritability)-and whether these effects and their fitness consequences are sex-specific-is essential to gain insights into the evolution of sexual dimorphism and sexual conflicts. We used 20+ years of data to study the sources of variation in adult body mass and associated fitness consequences in a bird with biparental care, the Alpine swift (Tachymarptis melba). Swifts appear monomorphic to human observers, though subtle dimorphisms are present. We first investigated the effects of weather conditions on adult body mass using a sliding window analysis approach. We report a positive effect of temperature and a negative effect of rainfall on adult body mass, as expected for an aerial insectivorous bird. We then quantified the additive genetic variance and heritability of body mass in both sexes and assessed the importance of genetic constraints on mass evolution by estimating the cross-sex genetic correlation. Heritability was different from zero in both sexes at ~0.30. The positive cross-sex genetic correlation and comparable additive genetic variance between the sexes suggest the possibility for evolutionary constraints when it comes to body mass. Finally, we assessed the sex-specific selection on adjusted body mass using multiple fitness components. We report directional positive and negative selection trending towards stabilizing and diversifying selection on females and males respectively in relation to the weighted proportion of surviving fledglings. Overall, these results suggest that while body mass may be able to respond to environmental conditions and evolve, genetic constraints would result in similar changes in both sexes or an overall absence of response to selection. It remains unclear whether the weak (1%) dimorphism in Alpine swift body mass we report is simply a result of the similar fitness peaks between the sexes or of genetic constraints.

Recent immigrants alter the quantitative genetic architecture of paternity in song sparrows.

Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection, and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multiyear pedigree, pairing, and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex-specific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances, and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.

Strong and weak cross-sex correlations govern the quantitative-genetic architecture of social group choice in Drosophila melanogaster.

When genotypes differ in niche-constructing traits, genotypes are expected to differ in which environments they experience, providing a novel causal relationship between genotypes, environments, and behavior. Such genetic variation in niche construction (or, more precisely, environment construction) is predicted to be especially important for social environments, yet the quantitative-genetic parameters governing such variation are still poorly understood. Here, we examine genetic variation and cross-sex genetic correlations for social environment-constructing behaviors. We focus on whether genetic variation in patch use-the tendency to spend time near food patches where conspecifics may be present-and group-size preference-the specific group size chosen when individuals are affiliating-is correlated or decoupled across sexes in the fruit fly, Drosophila melanogaster. Across three choice treatments, we find genotype and sex differences in how much time individuals spend near patches, and which group sizes they prefer. We find that the genetic basis of patch use is strongly coupled across sexes, whereas the genetic basis of group-size preference is completely decoupled across sexes. We discuss how these findings augment and complicate our understanding of the evolutionary genetics of social behaviors.

Quantifying maladaptation during the evolution of sexual dimorphism.

Females and males have distinct trait optima, resulting in selection for sexual dimorphism. However, most traits have strong cross-sex genetic correlations, which constrain evolutionary divergence between the sexes and lead to protracted periods of maladaptation during the evolution of sexual dimorphism. While such constraints are thought to be costly in terms of individual and population fitness, it remains unclear how severe such costs are likely to be. Building upon classical models for the 'cost of selection' in changing environments (sensu Haldane), we derived a theoretical expression for the analogous cost of evolving sexual dimorphism; this cost is a simple function of genetic (co)variances of female and male traits and sex differences in trait optima. We then conducted a comprehensive literature search, compiled quantitative genetic data from a diverse set of traits and populations, and used them to quantify costs of sexual dimorphism in the light of our model. For roughly 90% of traits, costs of sexual dimorphism appear to be modest, and comparable to the costs of fixing one or a few beneficial substitutions. For the remaining traits (approx. 10%), sexual dimorphism appears to carry a substantial cost-potentially orders of magnitude greater than costs of selection during adaptation to environmental changes.

Sex-specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding.

Quantifying sex-specific additive genetic variance (VA ) in fitness, and the cross-sex genetic correlation (rA ), is prerequisite to predicting evolutionary dynamics and the magnitude of sexual conflict. Further, quantifying VA and rA in underlying fitness components, and genetic consequences of immigration and resulting gene flow, is required to identify mechanisms that maintain VA in fitness. However, these key parameters have rarely been estimated in wild populations experiencing natural environmental variation and immigration. We used comprehensive pedigree and life-history data from song sparrows (Melospiza melodia) to estimate VA and rA in sex-specific fitness and underlying fitness components, and to estimate additive genetic effects of immigrants alongside inbreeding depression. We found evidence of substantial VA in female and male fitness, with a moderate positive cross-sex rA . There was also substantial VA in male but not female adult reproductive success, and moderate VA in juvenile survival but not adult annual survival. Immigrants introduced alleles with negative additive genetic effects on local fitness, potentially reducing population mean fitness through migration load, but alleviating expression of inbreeding depression. Our results show that VA for fitness can be maintained in the wild, and be broadly concordant between the sexes despite marked sex-specific VA in reproductive success.

Cross-sex genetic correlation does not extend to sexual size dimorphism in spiders.

Males and females are often subjected to different selection pressures for homologous traits, resulting in sex-specific optima. Because organismal attributes usually share their genetic architectures, sex-specific selection may lead to intralocus sexual conflict. Evolution of sexual dimorphism may resolve this conflict, depending on the degree of cross-sex genetic correlation (r MF) and the strength of sex-specific selection. In theory, high r MF implies that sexes largely share the genetic base for a given trait and are consequently sexually monomorphic, while low r MF indicates a sex-specific genetic base and sexual dimorphism. Here, we broadly test this hypothesis on three spider species with varying degrees of female-biased sexual size dimorphism, Larinioides sclopetarius (sexual dimorphism index, SDI = 0.85), Nuctenea umbratica (SDI = 0.60), and Zygiella x-notata (SDI = 0.46). We assess r MF via same-sex and opposite-sex heritability estimates. We find moderate body mass heritability but no obvious patterns in sex-specific heritability. Against the prediction, the degree of sexual size dimorphism is unrelated to the relative strength of same-sex versus opposite-sex heritability. Our results do not support the hypothesis that sexual size dimorphism is negatively associated with r MF. We conclude that sex-specific genetic architecture may not be necessary for the evolution of a sexually dimorphic trait.

The genetic basis for mating-induced sex differences in starvation resistance in Drosophila melanogaster.

Multiple genetic and environmental factors interact to influence starvation resistance, which is an important determinant of fitness in many organisms, including Drosophila melanogaster. Recent studies have revealed that mating can alter starvation resistance in female D. melanogaster, but little is known about the behavioral and physiological mechanisms underlying such mating-mediated changes in starvation resistance. In the present study, we first investigated whether the effect of mating on starvation resistance is sex-specific in D. melanogaster. As indicated by a significant sex×mating status interaction, mating increased starvation resistance in females but not in males. In female D. melanogaster, post-mating increase in starvation resistance was mainly attributed to increases in food intake and in the level of lipid storage relative to lean body weight. We then performed quantitative genetic analysis to estimate the proportion of the total phenotypic variance attributable to genetic differences (i.e., heritability) for starvation resistance in mated male and female D. melanogaster. The narrow-sense heritability (h(2)) of starvation resistance was 0.235 and 0.155 for males and females, respectively. Mated females were more resistant to starvation than males in all genotypes, but the degree of such sexual dimorphism varied substantially among genotypes, as indicated by a significant sex×genotype interaction for starvation resistance. Cross-sex genetic correlation was greater than 0 but less than l for starvation resistance, implying that the genetic architecture of this trait was partially shared between the two sexes. For both sexes, starvation resistance was positively correlated with longevity and lipid storage at genetic level. The present study suggests that sex differences in starvation resistance depend on mating status and have a genetic basis in D. melanogaster.

Testing the correlated response hypothesis for the evolution and maintenance of male mating preferences in Drosophila serrata.

Mate preferences are abundant throughout the animal kingdom with female preferences receiving the most empirical and theoretical attention. Although recent work has acknowledged the existence of male mate preferences, whether they have evolved and are maintained as a direct result of selection on males or indirectly as a genetically correlated response to selection for female choice remains an open question. Using the native Australian species Drosophila serrata in which mutual mate choice occurs for a suite of contact pheromones (cuticular hydrocarbons or CHCs), we empirically test key predictions of the correlated response hypothesis. First, within the context of a quantitative genetic breeding design, we estimated the degree to which the trait values favoured by male and female choice are similar both phenotypically and genetically. The direction of sexual selection on male and female CHCs differed statistically, and the trait combinations that maximized male and female mating success were not genetically correlated, suggesting that male and female preferences target genetically different signals. Second, despite detecting significant genetic variance in female preferences, we found no evidence for genetic variance in male preferences and, as a consequence, no detectable correlation between male and female mating preferences. Combined, these findings are inconsistent with the idea that male mate choice in D. serrata is simply a correlated response to female choice. Our results suggest that male and female preferences are genetically distinct traits in this species and may therefore have arisen via different evolutionary processes.

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird.

Oxidative stress was recently demonstrated to affect several fitness-related traits and is now well recognized to shape animal life-history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross-sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free-living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross-sex genetic correlation in offspring resistance to oxidative stress by performing a split-nest cross-fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free-radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross-sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.