Rebecca Dean

The evolutionary ecology of pre- and post-meiotic sperm senescence

Male reproductive success is an extremely variable fitness component. Understanding the maintenance of this variation is a key challenge in evolutionary biology. An often neglected source of variation in male reproductive success is determined by age-dependent patterns of decline in sperm fitness. Two pathways mediate sperm senescence: pre-meiotic senescence of somatic and germ cells of the ageing male, and post-meiotic ageing of the spermatozoon. Recently, theoretical and empirical studies have highlighted wide-ranging implications of both pathways. We clarify different mechanisms of sperm senescence, outlining their distinct evolutionary implications for the male, the female and the zygote, and their influence on fundamental evolutionary processes, including the evolution of anisogamy, sexual conflict, sexual selection, and applied issues such as assisted conception.

Sexual selection drives evolution and rapid turnover of male gene expression

Significance Genes with different expression between males and females (sex-biased genes) show rapid rates of sequence and expression divergence in a range of taxa. These characteristics have led many to assume that sex-biased genes are the product of sexual selection and sexual conflict, but this assumption remains to be rigorously tested. Using a phylogenetically controlled analysis of birds that exhibit diverse levels of sexual selection, we show a rapid turnover in sex-biased gene expression primarily through evolution of male expression levels and that the degree of sexual selection predicts the proportion of male-biased genes but does not account for rates of coding sequence evolution. We also discuss the impact of allometry on gene expression studies, an issue rarely discussed in the literature. The profound and pervasive differences in gene expression observed between males and females, and the unique evolutionary properties of these genes in many species, have led to the widespread assumption that they are the product of sexual selection and sexual conflict. However, we still lack a clear understanding of the connection between sexual selection and transcriptional dimorphism, often termed sex-biased gene expression. Moreover, the relative contribution of sexual selection vs. drift in shaping broad patterns of expression, divergence, and polymorphism remains unknown. To assess the role of sexual selection in shaping these patterns, we assembled transcriptomes from an avian clade representing the full range of sexual dimorphism and sexual selection. We use these species to test the links between sexual selection and sex-biased gene expression evolution in a comparative framework. Through ancestral reconstruction of sex bias, we demonstrate a rapid turnover of sex bias across this clade driven by sexual selection and show it to be primarily the result of expression changes in males. We use phylogenetically controlled comparative methods to demonstrate that phenotypic measures of sexual selection predict the proportion of male-biased but not female-biased gene expression. Although male-biased genes show elevated rates of coding sequence evolution, consistent with previous reports in a range of taxa, there is no association between sexual selection and rates of coding sequence evolution, suggesting that expression changes may be more important than coding sequence in sexual selection. Taken together, our results highlight the power of sexual selection to act on gene expression differences and shape genome evolution.

The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression

Males and females share most of their genomes, and differences between the sexes can therefore not evolve through sequence divergence in protein coding genes. Sexual dimorphism is instead restricted to occur through sex-specific expression and splicing of gene products. Evolution of sexual dimorphism through these mechanisms should, however, also be constrained when the sexes share the genetic architecture for regulation of gene expression. Despite these obstacles, sexual dimorphism is prevalent in the animal kingdom and commonly evolves rapidly. Here, we ask whether the genetic architecture of gene expression is plastic and easily molded by sex-specific selection, or if sexual dimorphism evolves rapidly despite pervasive genetic constraint. To address this question, we explore the relationship between the intersexual genetic correlation for gene expression (rMF), which captures how independently genes are regulated in the sexes, and the evolution of sex-biased gene expression. Using transcriptome data from Drosophila melanogaster, we find that most genes have a high rMF and that genes currently exposed to sexually antagonistic selection have a higher average rMF than other genes. We further show that genes with a high rMF have less pronounced sex-biased gene expression than genes with a low rMF within D. melanogaster and that the strength of the rMF in D. melanogaster predicts the degree to which the sex bias of a genes expression has changed between D. melanogaster and six other species in the Drosophila genus. In sum, our results show that a shared genome constrains both short- and long-term evolution of sexual dimorphism.

The measure and significance of Bateman's principles

Batemans principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Batemans principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Batemans principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Batemans principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.

Male reproductive senescence causes potential for sexual conflict over mating.

The realization that senescence, age-dependent declines in survival and reproductive performance, pervades natural populations has brought its evolutionary significance into sharper focus. However, reproductive senescence remains poorly understood because it is difficult to separate male and female mechanisms underpinning reproductive success. We experimentally investigated male reproductive senescence in feral fowl, Gallus gallus domesticus, where socially dominant males monopolize access to females and the ejaculates of multiple males compete for fertilization. We detected the signal of senescence on multiple determinants of male reproductive success. The effect of age on status was dependent upon the intensity of intrasexual competition: old males were less likely to dominate male-biased groups where competition is intense but were as likely as young males to dominate female-biased groups. Mating and fertilization success declined sharply with male age largely as a result of population-level patterns. These age-dependent declines translated into sexually antagonistic payoffs: old males fertilized more eggs when they were dominant, but this resulted in females suffering a drastic reduction in fertility. Thus, male senescence causes potential for sexual conflict over mating, and the intensity of this conflict is modulated socially, by the probability of old males dominating reproductive opportunities.

How to make a sex chromosome

Sex chromosomes can evolve once recombination is halted between a homologous pair of chromosomes. Owing to detailed studies using key model systems, we have a nuanced understanding and a rich review literature of what happens to sex chromosomes once recombination is arrested. However, three broad questions remain unanswered. First, why do sex chromosomes stop recombining in the first place? Second, how is recombination halted? Finally, why does the spread of recombination suppression, and therefore the rate of sex chromosome divergence, vary so substantially across clades? In this review, we consider each of these three questions in turn to address fundamental questions in the field, summarize our current understanding, and highlight important areas for future work.

The Risk and Intensity of Sperm Ejection in Female Birds

The way females utilize the gametes of different males has important consequences for sexual selection, sexual conflict, and intersexual coevolution in natural populations. However, patterns of sperm utilization by females are difficult to demonstrate, and their functional significance remains unclear. Here, we experimentally study sperm ejection in the fowl Gallus gallus domesticus, where females eject preferentially the sperm of socially subordinate males. We study two measures of sperm ejection, (i) the probability that an ejaculate is ejected (“risk”) and (ii) the proportion of semen ejected (“intensity”), and show that both measures are strongly nonrandom with respect to characteristics of the ejaculate, the male, and the female. Sperm ejection neutralized on average 80% of an ejaculate, and while larger ejaculates suffered a higher ejection risk, smaller ejaculates suffered more intense ejection. After controlling for ejaculate volume, we found socially subdominant males suffered higher ejection intensity. After controlling for male and ejaculate effects, we found ejection risk increased and intensity declined as females mated with successive males. Collectively, these results reveal that sperm ejection risk and intensity are at least partly actively caused by female behavior and generate independent selective pressures on male and ejaculate phenotypes.

The role of sex chromosomes in sexual dimorphism: discordance between molecular and phenotypic data

In addition to initial sex determination, genes on the sex chromosomes are theorized to play a particularly important role in phenotypic differences between males and females. Sex chromosomes in many species display molecular signatures consistent with these theoretical predictions, particularly through sex‐specific gene expression. However, the phenotypic implications of this molecular signature are unresolved, and the role of the sex chromosomes in quantitative genetic studies of phenotypic sex differences is largely equivocal. In this article, we examine molecular and phenotypic data in the light of theoretical predictions about masculinization and feminization of the sex chromosomes. Additionally, we discuss the role of genetic and regulatory complexities in the genome–phenotype relationship, and ultimately how these affect the overall role of the sex chromosomes in sex differences.

Positive Selection Underlies Faster-Z Evolution of Gene Expression in Birds

The elevated rate of evolution for genes on sex chromosomes compared with autosomes (Fast-X or Fast-Z evolution) can result either from positive selection in the heterogametic sex or from nonadaptive consequences of reduced relative effective population size. Recent work in birds suggests that Fast-Z of coding sequence is primarily due to relaxed purifying selection resulting from reduced relative effective population size. However, gene sequence and gene expression are often subject to distinct evolutionary pressures; therefore, we tested for Fast-Z in gene expression using next-generation RNA-sequencing data from multiple avian species. Similar to studies of Fast-Z in coding sequence, we recover clear signatures of Fast-Z in gene expression; however, in contrast to coding sequence, our data indicate that Fast-Z in expression is due to positive selection acting primarily in females. In the soma, where gene expression is highly correlated between the sexes, we detected Fast-Z in both sexes, although at a higher rate in females, suggesting that many positively selected expression changes in females are also expressed in males. In the gonad, where intersexual correlations in expression are much lower, we detected Fast-Z for female gene expression, but crucially, not males. This suggests that a large amount of expression variation is sex-specific in its effects within the gonad. Taken together, our results indicate that Fast-Z evolution of gene expression is the product of positive selection acting on recessive beneficial alleles in the heterogametic sex. More broadly, our analysis suggests that the adaptive potential of Z chromosome gene expression may be much greater than that of gene sequence, results which have important implications for the role of sex chromosomes in speciation and sexual selection.

Experimental evolution of a novel sexually antagonistic allele.

Evolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual conflict is emerging as a potentially fundamental factor for the genetic architecture of fitness, with important consequences for evolutionary processes. However, no study to date has directly experimentally tested the evolutionary fate of a sexually antagonistic allele. Using genetic constructs to manipulate female fecundity and male mating success, we engineered a novel sexually antagonistic allele (SAA) in Drosophila melanogaster. The SAA is nearly twice as costly to females as it is beneficial to males, but the harmful effects to females are recessive and X-linked, and thus are rarely expressed when SAA occurs at low frequency. We experimentally show how the evolutionary dynamics of the novel SAA are qualitatively consistent with the predictions of population genetic models: SAA frequency decreases when common, but increases when rare, converging toward an equilibrium frequency of ∼8%. Furthermore, we show that persistence of the SAA requires the mating advantage it provides to males: the SAA frequency declines towards extinction when the male advantage is experimentally abolished. Our results empirically demonstrate the dynamics underlying the evolutionary fate of a sexually antagonistic allele, validating a central assumption of intralocus sexual conflict theory: that variation in fitness-related traits within populations can be maintained via sex-linked sexually antagonistic loci.