POSITIVE SELECTION DRIVES FASTER‐Z EVOLUTION IN SILKMOTHS

Genes linked to X or Z chromosomes, which are hemizygous in the heterogametic sex, are predicted to evolve at different rates than those on autosomes. This “faster‐X effect” can arise either as a consequence of hemizygosity, which leads to more efficient selection for recessive beneficial mutations in the heterogametic sex, or as a consequence of reduced effective population size of the hemizygous chromosome, which leads to increased fixation of weakly deleterious mutations due to genetic drift. Empirical results to date suggest that, while the overall pattern across taxa is complicated, systems with male heterogamy show a faster‐X effect attributable to more efficient selection, whereas the faster‐Z effect in female‐heterogametic taxa is attributable to increased drift. To test the generality of the faster‐Z pattern seen in birds and snakes, we sequenced the genome of the lepidopteran silkmoth Bombyx huttoni. We show that silkmoths experience faster‐Z evolution, but unlike in birds and snakes, the faster‐Z effect appears to be attributable to more efficient positive selection. These results suggest that female heterogamy alone is unlikely to explain the reduced efficacy of selection on vertebrate Z chromosomes. It is likely that many factors, including differences in overall effective population size, influence Z chromosome evolution.     

Demographic stochasticity, allee effects, and extinction: the influence of mating system and sex ratio

Demographic stochasticity has a substantial influence on the growth of small populations and consequently on their extinction risk. Mating system is one of several population characteristics that may affect this. We use a stochastic pair-formation model to investigate the combined effects of mating system, sex ratio, and population size on demographic stochasticity and thus on extinction risk. Our model is designed to accommodate a continuous range of mating systems and sex ratios as well as several levels of stochasticity. We show that it is not mating system alone but combinations of mating system and sex ratio that are important in shaping the stochastic dynamics of populations. Specifically, polygyny has the potential to give a high demographic variance and to lower the stochastic population growth rate substantially, thus also shortening the time to extinction, but the outcome is highly dependent on the sex ratio. In addition, population size is shown to be important. We find a stochastic Allee effect that is amplified by polygyny. Our results demonstrate that both mating system and sex ratio must be considered in conservation planning and that appreciating the role of stochasticity is key to understanding their effects.     

Accelerated evolution of sex chromosomes in aphids, an x0 system

Sex chromosomes play a role in many important biological processes, including sex determination, genomic conflicts, imprinting, and speciation. In particular, they exhibit several unusual properties such as inheritance pattern, hemizygosity, and reduced recombination, which influence their response to evolutionary factors (e.g., drift, selection, and demography). Here, we examine the evolutionary forces driving X chromosome evolution in aphids, an XO system where females are homozygous (XX) and males are hemizygous (X0) at sex chromosomes. We show by simulations that the unusual mode of transmission of the X chromosome in aphids, coupled with cyclical parthenogenesis, results in similar effective population sizes and predicted levels of genetic diversity for X chromosomes and autosomes under neutral evolution. These results contrast with expectations from standard XX/XY or XX/X0 systems (where the effective population size of the X is three-fourths that of autosomes) and have deep consequences for aphid X chromosome evolution. We then localized 52 microsatellite markers on the X and 351 on autosomes. We genotyped 167 individuals with 356 of these loci and found similar levels of allelic richness on the X and on the autosomes, as predicted by our simulations. In contrast, we detected higher dN and dN/dS ratio for X-linked genes compared with autosomal genes, a pattern compatible with either positive or relaxed selection. Given that both types of chromosomes have similar effective population sizes and that the single copy of the X chromosome of male aphids exposes its recessive genes to selection, some degree of positive selection seems to best explain the higher rates of evolution of X-linked genes. Overall, this study highlights the particular relevance of aphids to study the evolutionary factors driving sex chromosomes and genome evolution.     

Effective size of density‐dependent two‐sex populations: the effect of mating systems

Density dependence in vital rates is a key feature affecting temporal fluctuations of natural populations. This has important implications for the rate of random genetic drift. Mating systems also greatly affect effective population sizes, but knowledge of how mating system and density regulation interact to affect random genetic drift is poor. Using theoretical models and simulations, we compare N_e in short‐lived, density‐dependent animal populations with different mating systems. We study the impact of a fluctuating, density‐dependent sex ratio and consider both a stable and a fluctuating environment. We find a negative relationship between annual N_e/N and adult population size N due to density dependence, suggesting that loss of genetic variation is reduced at small densities. The magnitude of this decrease was affected by mating system and life history. A male‐biased, density‐dependent sex ratio reduces the rate of genetic drift compared to an equal, density‐independent sex ratio, but a stochastic change towards male bias reduces the N_e/N ratio. Environmental stochasticity amplifies temporal fluctuations in population size and is thus vital to consider in estimation of effective population sizes over longer time periods. Our results on the reduced loss of genetic variation at small densities, particularly in polygamous populations, indicate that density regulation may facilitate adaptive evolution at small population sizes.     

EFFECTIVE POPULATION SIZE AND THE FASTER-X EFFECT: AN EXTENDED MODEL

Current models of X-linked and autosomal evolutionary rates often assume that the effective population size of the X chromosome ( N_eX ) is equal to three-quarters of the autosomal population size ( N_eA ). However, polymorphism studies of Drosophila melanogaster and D. simulans suggest that there are often significant deviations from this value. We have computed fixation rates of beneficial and deleterious mutations at X - linked and autosomal sites when this occurs. We find that N_eX/N_eA is a crucial parameter for the rates of evolution of X-linked sites compared to autosomal sites. Faster-X evolution due to the fixation of beneficial mutations can occur under a much wider range of levels of dominance when N_eX/N_eA > ³/₄. We also examined various parameters that are known to influence the rates of evolution at X-linked and autosomal sites, such as different mutation rates in males and females and mutations that are sexually antagonistic, to determine which cases can lead to faster-X evolution. We show that, when the rate of nonsynonymous evolution is normalized by the rate of neutral evolution, a sex difference in mutation rate has no influence on the conditions for faster-X evolution.     

Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a “social syndrome,” that includes cooperative breeding, reproductive skew, primary female‐biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short‐term benefits but come with long‐term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD‐sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister‐species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within‐population diversity were sixfold to 10‐fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species‐wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species‐wide genetic diversity of social species was 5–8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.     

Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms

It is usually posited that the most important factors contributing to sex chromosome evolution in diploids are the suppression of meiotic recombination and the asymmetry that results from one chromosome (the Y) being permanently heterozygous and the other (the X) being homozygous in half of the individuals involved in mating. To distinguish between the roles of these two factors, it would be valuable to compare sex chromosomes in diploid-mating organisms and organisms where mating compatibility is determined in the haploid stage. In this latter group, no such asymmetry occurs because the sex chromosomes are equally heterozygous. Here we show in the fungus Microbotryum violaceum that the chromosomes carrying the mating-type locus, and thus determining haploid-mating compatibility, are rich in transposable elements, dimorphic in size, and carry unequal densities of functional genes. Through analysis of available complete genomes, we also show that M. violaceum is, remarkably, more similar to humans and mice than to yeast, nematodes, or fruit flies with regard to the differential accumulation of transposable elements in the chromosomes determining mating compatibility vs. the autosomes. We conclude that restricted recombination, rather than asymmetrical sheltering, hemizygosity, or dosage compensation, is sufficient to account for the common sex chromosome characteristics.     

Sperm competition and the dynamics of X chromosome drive: stability and extinction

Several empirical studies of sperm competition in populations polymorphic for a driving X chromosome have revealed that Sex-ratio males (those carrying a driving X) are at a disadvantage relative to Standard males. Because the frequency of the driving X chromosome determines the population-level sex ratio and thus alters male and female mating rates, the evolutionary consequences of sperm competition for sex chromosome meiotic drive are subtle. As the SR allele increases in frequency, the ratio of females to males also increases, causing an increase in the male mating rate and a decrease in the female mating rate. While the former change may exacerbate the disadvantage of Sex-ratio males during sperm competition, the latter change decreases the incidence of sperm competition within the population. We analyze a model of the effects of sperm competition on a driving X chromosome and show that these opposing trends in male and female mating rates can result in two coexisting locally stable equilibria, one corresponding to a balanced polymorphism of the SR and ST alleles and the second to fixation of the ST allele. Stochastic fluctuations of either the population sex ratio or the SR frequency can then drive the population away from the balanced polymorphism and into the basin of attraction for the second equilibrium, resulting in fixation of the SR allele and extinction of the population.     

Dynamic linkage relationships to the mating‐type locus in automictic fungi of the genus Microbotryum

Regions of the chromosomes determining mating compatibility in some fungi, including Microbotryum lychnidis‐dioicae and Neurospora tetrasperma, exhibit suppressed recombination similar to sex chromosomes in plants and animals, and recent studies have sought to apply basic theories of sex chromosome evolution to fungi. A phylogeny of the MTL1 locus in Microbotryum indicates that it has become part of the nonrecombining regions of the mating‐type chromosomes in multiple independent events, and that recombination may have been subsequently restored in some cases. This illustrates that fungal mating‐type chromosomes can exhibit linkage relationship that are quite dynamic, adding to the list of similarities to animal or plant sex chromosomes. However, fungi such as M. lychnidis‐dioicae and N. tetrasperma exhibit an automictic mating system, for which an alternate theoretical framework exists to explain the evolution of linkage with the mating‐type locus. This study encourages further comparative studies among fungi to evaluate the role of mating systems in determining the evolution of fungal mating‐type chromosomes.     

Heterogeneous Histories of Recombination Suppression on Stickleback Sex Chromosomes

How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X–Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.     

The sex chromosome system can influence the evolution of sex‐biased dispersal

Sex‐biased dispersal is a much‐discussed feature in literature on dispersal. Diverse hypotheses have been proposed to explain the evolution of sex‐biased dispersal, a difference in dispersal rate or dispersal distance between males and females. An early hypothesis has indicated that it may rely on the difference in sex chromosomes between males and females. However, this proposal was quickly rejected without a real assessment. We propose a new perspective on this hypothesis by investigating the evolution of sex‐biased dispersal when dispersal genes are sex‐linked, that is when they are located on the sex chromosomes. We show that individuals of the heterogametic sex disperse relatively more than do individuals of the homogametic sex when dispersal genes are sex‐linked rather than autosomal. Although such a sex‐biased dispersal towards the heterogametic sex is always observed in monogamous species, the mating system and the location of dispersal genes interact to modulate sex‐biased dispersal in monandry and polyandry. In the context of the multicausality of dispersal, we suggest that sex‐linked dispersal genes can influence the evolution of sex‐biased dispersal.     

Sex chromosome polymorphism in guppies

Sex chromosomes differ from autosomes by dissimilar gene content and, at a more advanced stage of their evolution, also in structure and size. This is driven by the divergence of the Y or W from their counterparts, X and Z, due to reduced recombination and the resulting degeneration as well as the accumulation of sex-specific and sexually antagonistic genes. A paradigmatic example for Y-chromosome evolution is found in guppies. In these fishes, conflicting data exist for a morphological and molecular differentiation of sex chromosomes. Using molecular probes and the previously established linkage map, we performed a cytogenetic analysis of sex chromosomes. We show that the Y chromosome has a very large pseudoautosomal region, which is followed by a heterochromatin block (HCY) separating the subtelomeric male-specific region from the rest of the chromosome. Interestingly, the size of the HCY is highly variable between individuals from different population. The largest HCY was found in one population of Poecilia wingei, making the Y almost double the size of the X and the largest chromosome of the complement. Comparative analysis revealed that the Y chromosomes of different guppy species are homologous and share the same structure and organization. The observed size differences are explained by an expansion of the HCY, which is due to increased amounts of repetitive DNA. In one population, we observed also a polymorphism of the X chromosome. We suggest that sex chromosome-linked color patterns and other sexually selected genes are important for maintaining the observed structural polymorphism of sex chromosomes.     

Adaptation to experimental alterations of the operational sex ratio in populations of Drosophila melanogaster

Theory predicts that males adapt to sperm competition by increasing their investment in testis mass to transfer larger ejaculates. Experimental and comparative data support this prediction. Nevertheless, the relative importance of sperm competition in testis size evolution remains elusive, because experiments vary only sperm competition whereas comparative approaches confound it with other variables, in particular male mating rate. We addressed the relative importance of sperm competition and male mating rate by taking an experimental evolution approach. We subjected populations of Drosophila melanogaster to sex ratios of 1:1, 4:1, and 10:1 (female:male). Female bias decreased sperm competition but increased male mating rate and sperm depletion. After 28 generations of evolution, males from the 10:1 treatment had larger testes than males from other treatments. Thus, testis size evolved in response to mating rate and sperm depletion, not sperm competition. Furthermore, our experiment demonstrated that drift associated with sex ratio distortion limits adaptation; testis size only evolved in populations in which the effect of sex ratio bias on the effective population size had been compensated by increasing the numerical size. We discuss these results with respect to reproductive evolution, genetic drift in natural and experimental populations, and consequences of natural sex ratio distortion.     

Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes

The self-fertile nematode worms Caenorhabditis elegans, C. briggsae, and C. tropicalis evolved independently from outcrossing male-female ancestors and have genomes 20-40% smaller than closely related outcrossing relatives. This pattern of smaller genomes for selfing species and larger genomes for closely related outcrossing species is also seen in plants. We use comparative genomics, including the first high quality genome assembly for an outcrossing member of the genus (C. remanei) to test several hypotheses for the evolution of genome reduction under a change in mating system. Unlike plants, it does not appear that reductions in the number of repetitive elements, such as transposable elements, are an important contributor to the change in genome size. Instead, all functional genomic categories are lost in approximately equal proportions. Theory predicts that self-fertilization should equalize the effective population size, as well as the resulting effects of genetic drift, between the X chromosome and autosomes. Contrary to this, we find that the self-fertile C. briggsae and C. elegans have larger intergenic spaces and larger protein-coding genes on the X chromosome when compared to autosomes, while C. remanei actually has smaller introns on the X chromosome than either self-reproducing species. Rather than being driven by mutational biases and/or genetic drift caused by a reduction in effective population size under self reproduction, changes in genome size in this group of nematodes appear to be caused by genome-wide patterns of gene loss, most likely generated by genomic adaptation to self reproduction per se.     

No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

The canonical model of sex‐chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (nonrecombinant Y haplotypes) coexist with both XY° males with proto‐Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex‐determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study finds no effect of sex‐chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs might result more from the differential expression of autosomal genes than from sex‐linked SA genes. Among‐male variance in sex‐chromosome differentiation seems better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X‐Y recombination in XY females), independent of sex‐linked SA genes.     

Mammalian X Chromosome Dosage Compensation: Perspectives From the Germ Line

Sex chromosomes are advantageous to mammals, allowing them to adopt a genetic rather than environmental sex determination system. However, sex chromosome evolution also carries a burden, because it results in an imbalance in gene dosage between females (XX) and males (XY). This imbalance is resolved by X dosage compensation, which comprises both X chromosome inactivation and X chromosome upregulation. X dosage compensation has been well characterized in the soma, but not in the germ line. Germ cells face a special challenge, because genome wide reprogramming erases epigenetic marks responsible for maintaining the X dosage compensated state. Here we explain how evolution has influenced the gene content and germ line specialization of the mammalian sex chromosomes. We discuss new research uncovering unusual X dosage compensation states in germ cells, which we postulate influence sexual dimorphisms in germ line development and cause infertility in individuals with sex chromosome aneuploidy.     

Ancestral and neo-sex chromosomes contribute to population divergence in a dioecious plant

Empirical evidence from several animal groups suggests sex chromosomes disproportionately contribute to reproductive isolation. This effect may be enhanced when sex chromosomes are associated with turnover of sex determination systems resulting from structural rearrangements to the chromosomes. We investigated these predictions in the dioecious plant Rumex hastatulus, which is composed of populations of two different sex chromosome cytotypes caused by an X-autosome fusion. Using population genomic analyses, we investigated the demographic history of R. hastatulus and explored the contributions of ancestral and neo-sex chromosomes to population genetic divergence. Our study revealed that the cytotypes represent genetically divergent populations with evidence for historical but not contemporary gene flow between them. In agreement with classical predictions, we found that the ancestral X chromosome was disproportionately divergent compared with the rest of the genome. Excess differentiation was also observed on the Y chromosome, even when we used measures of differentiation that control for differences in effective population size. Our estimates of the timing of the origin of neo-sex chromosomes in R. hastatulus are coincident with cessation of gene flow, suggesting that the chromosomal fusion event that gave rise to the origin of the XYY cytotype may have also contributed to reproductive isolation.     

Environmental stress maintains trioecy in nematode worms

Sex is determined by chromosomes in mammals but it can be influenced by the environment in many worms, crustaceans, and vertebrates. Despite this, there is little understanding of the relationship between ecology and the evolution of sexual systems. The nematode Auanema freiburgensis has a unique sex determination system in which individuals carrying one X chromosome develop into males while XX individuals develop into females in stress-free environments and self-fertile hermaphrodites in stressful environments. Theory predicts that trioecious populations with coexisting males, females, and hermaphrodites should be unstable intermediates in evolutionary transitions between mating systems. In this article, we study a mathematical model of reproductive evolution based on the unique life history and sex determination of A. freiburgensis. We develop the model in two scenarios, one where the relative production of hermaphrodites and females is entirely dependent on the environment and one based on empirical measurements of a population that displays incomplete, “leaky” environmental dependence. In the first scenario environmental conditions can push the population along an evolutionary continuum and result in the stable maintenance of multiple reproductive systems. The second “leaky” scenario results in the maintenance of three sexes for all environmental conditions. Theoretical investigations of reproductive system transitions have focused on the evolutionary costs and benefits of sex. Here, we show that the flexible sex determination system of A. freiburgensis may contribute to population-level resilience in the microscopic nematode's patchy, ephemeral natural habitat. Our results demonstrate that life history, ecology, and environment may play defining roles in the evolution of sexual systems.