Sex‐antagonistic genes, XY recombination and feminized Y chromosomes

Abstract

The canonical model of sex-chromosome evolution predicts that sex-antagonistic (SA) genes play an instrumental role in the arrest of XY recombination and ensuing Y chromosome degeneration. Although this model might account for the highly differentiated sex chromosomes of birds and mammals, it does not fit the situation of many lineages of fish, amphibians or nonavian reptiles, where sex chromosomes are maintained homomorphic through occasional XY recombination and/or high turnover rates. Such situations call for alternative explanatory frameworks. A crucial issue at stake is the effect of XY recombination on the dynamics of SA genes and deleterious mutations. Using individual-based simulations, we show that a complete arrest of XY recombination actually benefits females, not males. Male fitness is maximized at different XY recombination rates depending on SA selection, but never at zero XY recombination. This should consistently favour some level of XY recombination, which in turn generates a recombination load at sex-linked SA genes. Hill-Robertson interferences with deleterious mutations also impede the differentiation of sex-linked SA genes, to the point that males may actually fix feminized phenotypes when SA selection and XY recombination are low. We argue that sex chromosomes might not be a good localization for SA genes, and sex conflicts seem better solved through the differential expression of autosomal genes.

Sex-dependent dominance maintains migration supergene in rainbow trout

“…The Y chromosome was not enriched for male benefit genes (178/919 Y genes compared to 9005/47415 autosomal genes, -log2 transcripts per million (TPM), one-tailed Fisher’s exact test p = 0.513, Figure 4e), consistent with X-Y recombination and/or frequent turnover preventing enrichment of male benefit genes. Conversely, low recombination between X and Y with weak sexual antagonism can lead to feminisation of the Y chromosome 8 . However, there was also no enrichment in female benefit genes (173/919 Y genes compared to 8091/47415 autosomal genes, -log2 TPM, Fisher’s exact test p = 0.29), with the same proportion of both testis and oocyte genes as expected if they were evenly distributed across the chromosomes (18-19 %, Figure 4e).…”

“…While this model explains sexual conflict resolution in some species, many taxa lack differentiated sex chromosomes 5 , and how sexually antagonistic variation is maintained in these species is largely unknown 4,7 . Additionally, recent theoretical work has predicted that sexual conflict may be better resolved by autosomal variation 8 , a prediction supported by genome-wide mapping of sexually antagonistic polymorphisms 3 . Thus, mechanisms that maintain sexual conflict polymorphisms on the autosomes must be common, yet the only known genetic mechanism for maintaining sexually antagonistic polymorphisms on autosomes, sex-dependent dominance 7,9 , has been observed only once for a single gene 4 .…”

“…Balancing selection can facilitate the evolution of novel dominance patterns and these, along with epistasis, are an important features of inversion polymorphism 16,17 . Typical of taxa with homomorphic sex chromosomes 5,8,18 , salmonids have undergone frequent sex chromosome turnover 19 , and sex-reversed males (XY females) have been suggested to occur 20,21 , both of which are predicted to limit divergence of the sex chromosomes 5,22 and their ability to accumulate and protect sexual conflict polymorphisms 8,18 . Here we generate a chromosome-level genome assembly for rainbow trout and use it to identify a large autosomal inversion supergene influencing sexually antagonistic migratory tendency with sex-dependent dominance.…”

Evolutionary dynamics of sex chromosomes of paleognathous birds

“…Simulations suggest that complete recombination suppression can sometimes be harmful to the heterogametic sex, and sex chromosomes are not favorable locations for sexually antagonistic alleles in many lineages (Cavoto et al 2017). An alternative evolutionary explanation for loss of recombination in the heterogametic sex is then needed.…”

Genomic architecture and evolutionary conflict drive allele-specific expression in the social supergene of the red fire ant

“…Studies focusing on young sex chromosome systems, however, suggest that the role of evolutionary conflict in driving sex chromosome evolution has been overestimated (19)(20)(21)(22)(23)(24). Instead, sex chromosome evolution could be driven mostly by processes unrelated to phenotypic differences between sexes (5,25,26). For example, gene-specific dosage compensation can be favored in response to mutations that change coding sequences (27) or expression levels (28,29) in the non-recombining variant.…”