Development of a Set of Microsatellite Markers to Investigate Sexually Antagonistic Selection in the Invasive Ant Nylanderia fulva

Sexually antagonistic selection (SAS) occurs when distinct alleles are differentially selected in each sex. In the invasive tawny crazy ant, Nylanderia fulva, a genomic region is under SAS, while the rest of the genome is randomly selected in males and females. In this study, we designed a suite of 15 microsatellite markers to study the origin and evolution of SAS in N. fulva. These SAS markers were polymorphic, with allelic frequencies that are highly different between males and females. All haploid males carry only a subset of the alleles present in the population, while females are reliably heterozygous, with one allele from the male gene pool and a different allele inherited from their mother. In addition, we identified six polymorphic markers not associated with SAS and six markers yielding consistent, yet monomorphic, amplification in the introduced range of this species. Reaction condition optimizations allowed all retained markers to be co-amplified in four PCR mixes. The SAS markers may be used to test for the strength and the extent of the genomic regions under SAS in both the native and introduced ranges of N. fulva, while the set of non-SAS loci may be used to assess the invasion route of this species. Overall, the application of these microsatellite markers will yield insights into the origin and evolution of SAS within and among species of the genus Nylanderia.

A neutral model for the loss of recombination on sex chromosomes

The loss of recombination between sex chromosomes has occurred repeatedly throughout nature, with important implications for their subsequent evolution. Explanations for this remarkable convergence have generally invoked only adaptive processes (e.g. sexually antagonistic selection); however, there is still little evidence for these hypotheses. Here we propose a model in which recombination on sex chromosomes is lost due to the neutral accumulation of sequence divergence adjacent to (and thus, in linkage disequilibrium with) the sex determiner. Importantly, we include in our model the fact that sequence divergence, in any form, reduces the probability of recombination between any two sequences. Using simulations, we show that, under certain conditions, a region of suppressed recombination arises and expands outwards from the sex-determining locus, under purely neutral processes. Further, we show that the rate and pattern of recombination loss are sensitive to the pre-existing recombination landscape of the genome and to sex differences in recombination rates, with patterns consistent with evolutionary strata emerging under some conditions. We discuss the applicability of these results to natural systems. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

In species with polygenic sex determination, multiple male- and female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are at stable equilibria is not yet resolved. Previous work demonstrated that polygenic sex determination is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider polygenic sex determination systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the alleles under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain polygenic sex determination under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes are more likely to maintain polygenic sex determination than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain polygenic sex determination tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain polygenic sex determination tend to have sexually antagonistic multi-chromosomal genotypes, but the individual proto-sex chromosomes do not have sexually antagonistic effects. These results demonstrate that sexual antagonism can be an emergent property of the multi-chromosome genotype without individual sexually antagonistic chromosomes. My results further illustrate how the dominance of fitness effects has consequences for both the likelihood that polygenic sex determination will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism.

The genetic architecture of sexual dimorphism in the mossCeratodon purpureus

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the mossCeratodon purpureus.We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (rmf) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (GfandGm, respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrixBcontained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.

Establishment of a new sex-determining allele driven by sexually antagonistic selection

The turnover of sex-determining loci has repeatedly occurred in a number of species, rather than having a diverged pair of sex chromosomes. We model the turnover process by considering a linked locus under sexually antagonistic selection. The entire process of a turnover may be divided into two phases, which are referred to as the stochastic and deterministic phases. The stochastic phase is when a new sex-determining allele just arises and is still rare and random genetic drift plays an important role. In the deterministic phase, the new allele further increases in frequency by positive selection. The theoretical results currently available are for the deterministic phase, which demonstrated that a turnover of a newly arisen sex-determining locus could benefit from selection at a linked locus under sexually antagonistic selection, by assuming that sexually antagonistic selection works in a form of balancing selection. In this work, we provide a comprehensive theoretical description of the entire process from the stochastic phase to the deterministic phase. In addition to balancing selection, we explore several other modes of selection on the linked locus. Our theory allows us make a quantitative argument on the rate of turnover and the effect of the mode of selection at the linked locus. We also performed simulations to explore the pattern of polymorphism around the new sex-determining locus. We find that the pattern of polymorphism is informative to infer how selection worked through the turnover process.

Establishment of a new sex-determining allele driven by sexually antagonistic selection

ABSTRACTSome species undergo frequent turnovers of sex-determining locus, rather than having stable diverged sex chromosomes. In such species, how often turnover occurs is a fundamental evolutionary question. We model the process with considering a linked locus under sexually antagonistic selection. The entire process of a turnover may be divided into two phases, which are referred to as the stochastic and deterministic phases. The stochastic phase is when a new sex-determining allele just arises and is still rare and random genetic drift plays an important role. In the deterministic phase, the new allele further increases in frequency by positive selection. The theoretical results currently available are for the deterministic phase, which demonstrated that a turnover of a newly arisen sex determining locus could benefit from selection at a linked locus under sexually antagonistic selection, by assuming that sexually antagonistic selection works in a form of balancing selection. In this work, we provide a comprehensive theoretical description of the entire process from the stochastic phase to the deterministic phase. In addition to balancing selection, we explore several other modes of selection on the linked locus. Our theory allows us make a quantitative argument on the rate of turnover and the effect of the mode of selection at the linked locus. We also performed simulations to explore the pattern of polymorphism around the new sex determining locus. We find that the pattern of polymorphism is informative to infer how selection worked through the turnover process.

Why Do Some Sex Chromosomes Degenerate More Slowly Than Others? The Odd Case of Ratite Sex Chromosomes

The hallmark of sex chromosome evolution is the progressive suppression of recombination which leads to subsequent degeneration of the non-recombining chromosome. In birds, species belonging to the two major clades, Palaeognathae (including tinamous and flightless ratites) and Neognathae (all remaining birds), show distinctive patterns of sex chromosome degeneration. Birds are female heterogametic, in which females have a Z and a W chromosome. In Neognathae, the highly-degenerated W chromosome seems to have followed the expected trajectory of sex chromosome evolution. In contrast, among Palaeognathae, sex chromosomes of ratite birds are largely recombining. The underlying reason for maintenance of recombination between sex chromosomes in ratites is not clear. Degeneration of the W chromosome might have halted or slowed down due to a multitude of reasons ranging from selective processes, such as a less pronounced effect of sexually antagonistic selection, to neutral processes, such as a slower rate of molecular evolution in ratites. The production of genome assemblies and gene expression data for species of Palaeognathae has made it possible, during recent years, to have a closer look at their sex chromosome evolution. Here, we critically evaluate the understanding of the maintenance of recombination in ratites in light of the current data. We conclude by highlighting certain aspects of sex chromosome evolution in ratites that require further research and can potentially increase power for the inference of the unique history of sex chromosome evolution in this lineage of birds.

Detection of sexually antagonistic transmission distortions in trio datasets

ABSTRACTSex dimorphisms are widespread in animals and plants, for morphological as well as physiological traits. Understanding the genetic basis of sex dimorphism and its evolution is crucial for understanding biological differences between the sexes. Genetic variants with sex-antagonistic effects on fitness are expected to segregate in populations at the early phases of sexual dimorphism emergence. Detecting such variants is notoriously difficult, and the few genome-scan methods employed so far have limited power and little specificity. Here, we propose a new framework to detect a signature of sexually antagonistic selection. We rely on trio datasets where sex-biased transmission distortions can be directly tracked from parents to offspring, and allows identifying signal of sexually antagonistic transmission distortions in genomic regions. We report the genomic location and recombination pattern surrounding 66 regions detected as potentially under sexually antagonist selection. We find an enrichment of genes associated with embryonic development within these regions. Last, we highlight two candidates regions for sexually antagonistic selection in humans.

The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

In species with polygenic sex determination, multiple male- and/or female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are stable equilibria is not yet resolved. Previous work demonstrated that polygenic sex determination is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider polygenic sex determination systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the variants under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain polygenic sex determination under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes in males are more likely to maintain polygenic sex determination than dominant, recessive, or additive fitness effects. I also found that additive fitness effects that maintain polygenic sex determination have the strongest signatures of sexually antagonistic selection, but there is also some evidence for sexually antagonism when fitness effects of proto-Y chromosomes are dominant or recessive. More generally, these results suggest that the expected effect of sexually antagonistic selection on the maintenance of genetic variation in natural populations will depend on whether the alleles are sex-linked and the dominance of their fitness effects.

A mobile sex-determining region, male-specific haplotypes, and rearing environment influence age at maturity in Chinook salmon

Variation in age at maturity is an important contributor to life history and demographic variation within and among species. The optimal age at maturity can vary by sex, and the ability of each sex to evolve towards its fitness optimum depends on the genetic architecture of maturation. Using GWAS of RAD sequencing data, we show that age at maturity in Chinook salmon exhibits sex-specific genetic architecture, with age at maturity in males governed by large (up to 20Mb) male-specific haplotypes. These regions showed no such effect in females. We also provide evidence for translocation of the sex-determining gene between two different chromosomes. This has important implications for sexually antagonistic selection, particularly that sex-linkage of adaptive genes may differ within and among populations based on chromosomal location of the sex-determining gene. Our findings will facilitate research into the genetic causes of shifting demography in Chinook salmon as well as a better understanding of sex-determination in this species and Pacific salmon in general.