Guppy Y chromosome integrity maintained by incomplete recombination suppression

The loss of recombination triggers divergence between the sex chromosomes and promotes degeneration of the sex-limited chromosome. Several livebearers within the genus Poecilia share a male-heterogametic sex chromosome system that is roughly 20 million years old, with extreme variation in the degree of Y chromosome divergence. In P. picta, the Y is highly degenerate and associated with complete X chromosome dosage compensation. In contrast, although recombination is restricted across almost the entire length of the sex chromosomes in P. reticulata and P wingei, divergence between the X and the Y chromosome is very low. This clade therefore offers a unique opportunity to study the forces that accelerate or hinder sex chromosome divergence. We used RNA-seq data from multiple families of both P. reticulata and P. wingei, the species with low levels of sex chromosome divergence, to differentiate X and Y coding sequence based on sex-limited SNP inheritance. Phylogenetic tree analyses reveal that occasional recombination has persisted between the sex chromosomes for much of their length, as X- and Y-linked sequences cluster by species instead of by gametolog. This incomplete recombination suppression maintains the extensive homomorphy observed in these systems. In addition, we see differences between the previously identified strata in the phylogenetic clustering of X-Y orthologs, with those that cluster by chromosome located in the older stratum, the region previously associated with the sex-determining locus. However, recombination arrest appears to have expanded throughout the sex chromosomes more gradually instead of through a stepwise process associated with inversions

Compensation of Dosage-Sensitive Genes on the Chicken Z Chromosome.

In many diploid species, sex determination is linked to a pair of sex chromosomes that evolved from a pair of autosomes. In these organisms, the degeneration of the sex-limited Y or W chromosome causes a reduction in gene dose in the heterogametic sex for X- or Z-linked genes. Variations in gene dose are detrimental for large chromosomal regions when they span dosage-sensitive genes, and many organisms were thought to evolve complete mechanisms of dosage compensation to mitigate this. However, the recent realization that a wide variety of organisms lack complete mechanisms of sex chromosome dosage compensation has presented a perplexing question: How do organisms with incomplete dosage compensation avoid deleterious effects of gene dose differences between the sexes? Here we use expression data from the chicken (Gallus gallus) to show that ohnologs, duplicated genes known to be dosage-sensitive, are preferentially dosage-compensated on the chicken Z chromosome. Our results indicate that even in the absence of a complete and chromosome wide dosage compensation mechanism, dosage-sensitive genes are effectively dosage compensated on the Z chromosome

Shared and species-specific patterns of nascent Y chromosome evolution in two guppy species

Sex chromosomes form once recombination is halted around the sex-determining locus between a homologous pair of chromosomes, resulting in a male-limited Y chromosome. We recently characterized the nascent sex chromosome system in the Trinidadian guppy (Poeciliareticulata). The guppy Y is one of the youngest animal sex chromosomes yet identified, and therefore offers a unique window into the early evolutionary forces shaping sex chromosome formation, particularly the rate of accumulation of repetitive elements and Y-specific sequence. We used comparisons between male and female genomes in P. reticulata and its sister species, Endler’s guppy (P. wingei), which share an ancestral sex chromosome, to identify male-specific sequences and to characterize the degree of differentiation between the X and Y chromosomes. We identified male-specific sequence shared between P. reticulata and P. wingei consistent with a small ancestral non-recombining region. Our assembly of this Y-specific sequence shows substantial homology to the X chromosome, and appears to be significantly enriched for genes implicated in pigmentation. We also found two plausible candidates that may be involved in sex determination. Furthermore, we found that the P. wingei Y chromosome exhibits a greater signature of repetitive element accumulation than the P. reticulata Y chromosome. This suggests that Y chromosome divergence does not necessarily correlate with the time since recombination suppression. Overall, our results reveal the early stages of Y chromosome divergence in the guppy

Phenotypic sexual dimorphism is associated with genomic signatures of resolved sexual conflict

Intra‐locus sexual conflict, where an allele benefits one sex at the expense of the other, has an important role in shaping genetic diversity of populations through balancing selection. However, the potential for mating systems to exert balancing selection through sexual conflict on the genome remains unclear. Furthermore, the nature and potential for resolution of sexual conflict across the genome has been hotly debated. To address this, we analysed de novo transcriptomes from six avian species, chosen to reflect the full range of sexual dimorphism and mating systems. Our analyses combine expression and population genomic statistics across reproductive and somatic tissue, with measures of sperm competition and promiscuity. Our results reveal that balancing selection is weakest in the gonad, consistent with the resolution of sexual conflict and evolutionary theory that phenotypic sex differences are associated with lower levels of ongoing conflict. We also demonstrate a clear link between variation in sexual conflict and levels of genetic variation across phylogenetic space in a comparative framework. Our observations suggest that this conflict is short‐lived, and is resolved via the decoupling of male and female gene expression patterns, with important implications for the role of sexual selection in adaptive potential and role of dimorphism in facilitating sex‐specific fitness optima

Recent sex chromosome divergence despite ancient dioecy in the willow Salix viminalis.

Sex chromosomes can evolve when recombination is halted between a pair of chromosomes, and this can lead to degeneration of the sex-limited chromosome. In the early stages of differentiation sex chromosomes are homomorphic, and even though homomorphic sex chromosomes are very common throughout animals and plants, we know little about the evolutionary forces shaping these types of sex chromosomes. We used DNA- and RNA-Seq data from females and males to explore the sex chromosomes in the female heterogametic willow, Salix viminalis, a species with ancient dioecy but with homomorphic sex chromosomes. We detected no major sex differences in read coverage in the SD region, indicating that the W region has not significantly degenerated. However, SNP densities in the SD region are higher in females compared to males, indicating very recent recombination suppression, followed by the accumulation of sex-specific SNPs. Interestingly, we identified two female-specific scaffolds that likely represent W-chromosome-specific sequence. We show that genes located in the SD region display a mild excess of male-biased expression in sex-specific tissue, and we use allele-specific gene expression analysis to show that this is the result of masculinization of expression on the Z chromosome rather than degeneration of female-expression on the W chromosome. Together, our results demonstrate that insertion of small DNA fragments and accumulation of sex-biased gene expression can occur before the detectable decay of the sex-limited chromosome

Evolution of dosage compensation under sexual selection differs between X and Z chromosomes.

Complete sex chromosome dosage compensation has more often been observed in XY than ZW species. In this study, using a population genetic model and the chicken transcriptome, we assess whether sexual conflict can account for this difference. Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex. Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation. Using expression variance as a measure of selection strength, we find that, as predicted by the model, dosage compensation in the chicken is most pronounced in genes that are under strong selection biased towards females. Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation

Signature of sexual conflict is actually conflict resolved

There has been substantial interest of late in using population genetic methods to study sexual conflict, where an allele increases the fitness of one sex at some cost to the other (Mank 2017). Population genomic scans for sexual conflict offer an important advance given the difficulties of identifying antagonistic alleles from more traditional methods, and could greatly increase our understanding of the extent and loci of sexual conflict

Constraint and divergence in the evolution of male and female recombination rates in fishes

Recombination is a fundamental feature of sexual reproduction across eukaryotes, yet recombination rates are highly variable both within and between species. In particular, sex differences in recombination rate between males and females (heterochiasmy) is more often the rule than the exception, but despite its prevalence the ultimate causes of global patterns of heterochiasmy remain unclear. Here, we assemble a comprehensive dataset of sex-specific recombination rate estimates for 61 fish species, and combine this with information on sex determination, fertilisation mode and sexual dimorphism to test competing theories for the causes and evolution of heterochiasmy. We find that sex differences in recombination rate are evolutionary labile, with frequent shifts in the direction and magnitude of heterochiasmy. This rapid turnover does not appear to be driven by simple neutral processes and is inconsistent with non-adaptive explanations for heterochiasmy, including biological sex differences in meiosis. However, while patterns of heterochiasmy across the phylogeny indicate a potential role for adaptive processes, we are unable to directly link variation in heterochiasmy with proxies for sexual selection or sexual conflict across species, indicating that these effects – if present – are either subtle or complex. Finally, we show evidence for correlated rates of recombination rate evolution between males and females, indicating the potential for genetic constraints and sexual conflict over the recombination landscape

Sperm competition shapes gene expression and sequence evolution in the ocellated wrasse.

Gene expression differences between males and females often underlie sexually dimorphic phenotypes, and the expression levels of genes that are differentially expressed between the sexes are thought to respond to sexual selection. Most studies on the transcriptomic response to sexual selection treat sexual selection as a single force, but postmating sexual selection in particular is expected to specifically target gonadal tissue. The three male morphs of the ocellated wrasse (Symphodus ocellatus) make it possible to test the role of postmating sexual selection in shaping the gonadal transcriptome. Nesting males hold territories and have the highest reproductive success, yet we detected feminization of their gonadal gene expression compared to satellite males. Satellite males are less brightly coloured and experience more intense sperm competition than nesting males. In line with postmating sexual selection affecting gonadal gene expression, we detected a more masculinized expression profile in satellites. Sneakers are the lowest quality males and showed both de-masculinization and de-feminization of gene expression. We also detected higher rates of gene sequence evolution of male-biased genes compared to unbiased genes, which could at least in part be explained by positive selection. Together, these results reveal the potential for postmating sexual selection to drive higher rates of gene sequence evolution and shape the gonadal transcriptome profile

A comparison of methodological approaches to the study of young sex chromosomes : a case study in Poecilia

Studies of sex chromosome systems at early stages of divergence are key to understanding the initial process and underlying causes of recombination suppression. However, identifying signatures of divergence in homomorphic sex chromosomes can be challenging due to high levels of sequence similarity between the X and the Y. Variations in methodological precision and underlying data can make all the difference between detecting subtle divergence patterns or missing them entirely. Recent efforts to test for X-Y sequence differentiation in the guppy have led to contradictory results. Here we apply different analytical methodologies to the same dataset to test for the accuracy of different approaches in identifying patterns of sex chromosome divergence in the guppy. Our comparative analysis reveals that the most substantial source of variation in the results of the different analyses lies in the reference genome used. Analyses using custom-made genome assemblies for the focal population or species successfully recover a signal of divergence across different methodological approaches. By contrast, using the distantly related Xiphophorus reference genome results in variable patterns, due to both sequence evolution and structural variations on the sex chromosomes between the guppy and Xiphophorus. Changes in mapping and filtering parameters can additionally introduce noise and obscure the signal. Our results illustrate how analytical differences can alter perceived results and we highlight best practices for the study of nascent sex chromosomes