Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Abstract

Once recombination is halted between the X and Y chromosome, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about variation in sex chromosome differentiation within clades. Here, we combined whole genome and transcriptome sequencing data to characterise the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged 30 mya. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata are largely homomorphic, with recombination persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely non-recombining and strikingly heteromorphic. ln addition to being highly divergent, the sex chromosome system in P. picta includes a neo-sex chromosome, the result of a fusion between the ancestral sex chromosome and part of chromosome 7. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of complete dosage compensation in this species, the first such documented case in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

How to identify sex chromosomes and their turnover

“…This step is key for establishing the identity of the sex chromosome pair via synteny‐based approaches with other species (see Box 1), as sex‐limited chromosomes are often highly degenerated which hinders attempts to infer orthology. Alternatively, the ratio of male to female reads aligned to a reference genome can be used to directly distinguish X from autosomal scaffolds (Darolti et al, ; Vicoso & Bachtrog, , ; Vicoso, Emerson, Zektser, Mahajan, & Bachtrog, ). For example, in an XY system, the male to female coverage ratio for autosomal and X scaffolds should be roughly 1 and 0.5 respectively.…”

“…For example, in nascent sex chromosomes with limited Y chromosome degeneration, Y‐linked genomic reads will map to the homologous region of the X in a female reference genome, resulting in elevated SNP density in males relative to females (Figure d). Therefore, elevated SNP density in the heterogametic sex can be used to infer sex‐linked regions when mapped to a reference genome generated from the homogametic sex (Darolti et al, ; Vicoso et al, ; Wright et al, ). In contrast, in regions where the Y has largely degenerated, we expect SNP density to be lower in males when mapped to a female genome as the X is effectively hemizygous in males (Rovatsos, Farkačová, Altmanová, Johnson Pokorná, & Kratochvíl, ; Rovatsos, Rehák, Velenský, & Kratochvíl, ; Rovatsos, Vukić, & Kratochvíl, ).…”

“…Finally, scaffolds with limited sex differences in polymorphism are probably autosomal or pseudoautosomal. Together, this rationale can be used not only to identify sex chromosomes at the intermediate stages of divergence, but also strata of different ages along the chromosome (Darolti et al, ; Wright et al, ) (Figure d). Contrasting SNP density between males and females is therefore a powerful approach to identify sex chromosomes or strata at the intermediate stages of X and Y (or Z and W) divergence.…”

“…Often this information is not available and therefore a permutation approach to estimate the null distribution of sex differences in SNP density across the genome is essential to identify regions with significantly elevated SNP density in the heterogametic sex (see Box 1). This method is most successful when combined with the coverage approach (Figure d) so that multiple, independent lines of evidence can be used to identify sex‐linked regions (Darolti et al, ; Shearn et al, ; Vicoso et al, ).…”

“…Much of the current work in this area involves species of fish, and we suggest future work should continue in these taxa due to the repeated origins of homomorphic sex chromosomes. Studying species or populations where there is variation in the extent of recombination suppression between sex chromosomes, as in Poeciliids (Bergero et al, ; Darolti et al, ; Wright et al, ), promises to be a fruitful avenue. A powerful approach would be targeting young sex chromosomes within a sex‐specific evolution framework to test whether sexually antagonistic mutations accumulate prior to recombination suppression (Ponnikas, Sigeman, Abbott, & Hansson, ).…”