Sex chromosomes have evolved independently many times throughout the eukaryotes, and represent a remarkable case of genomic convergence, as unrelated sex chromosomes share many properties across distant taxa. Sex chromosomes evolve after recombination is halted between a homologous pair of chromosomes, but little is known about why this process occurs. The most commonly accepted theory of sex chromosome evolution predicts that recombination will be selected against in the region between a sex-determining gene and a nearby gene with sex-specific effects. This paper was the first direct test of this long-standing theory. We used replicate guppy (Poecilia reticulata) populations with varying level of sexual selection. In each replicate, increased sexual selection has led to an expansion of the non-recombining region. Remarkably, this has occurred independently in each population, suggesting that sex chromosomes can form very quickly and despite considerable gene flow. This study therefore offers the first direct empirical evidence of the forces underlying sexual chromosome formation, and indicates that sexual selection is a major force of genome evolution. This work was published as Wright et al. Nature Communications 2017. We followed this up with a detailed molecular analysis of the sex chromosomes in these populations (Almeia et al. Molecular Biology and Evolution 2020), and we showed that the male-specific region of the Y chromosome has collected substantial coding content through recent gene duplications (Lin et al. Molecular Ecology 2022).
We then 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 20 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. 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.This was published as Darolti et al. Proceedings of the National Academy of Sciences 2019; Darolti et al. Genome Biology and Evolution 2020; Darolti et al. Journal of Evolutionary Biology 2022.
We also examined the role of the Y chromosome in guppy colouration using novel computational phenotyping approaches. Our results show that colour patterning itself is not Y-linked, contrary to long-standing paradigms, but that overall colouration does have significant Y effects. This was published as Morris et al. Proceedings of the Royal Society B, 2020. In contrast to guppies, we showed that the Y chromosome encodes the complex phenotypes of male para guppies, published as Sandkam et al. Nature Ecology and Evolution 2021.
A major focus of the project has been understanding the genetic basis of sex-specific phenotypes, and this has been a very productive avenue, including van der Bijl et al. Evolution Letters 2021; Cooney et al. Evolution 2021;Wright et al. Molecular Ecology 2019; Bloch et al. Nature Ecology and Evolution 2018; Wright et al. Evolution Letters 2018; Mank Nature Reviews Genetics 2017; Corral Lopez Science Advances 2017.
Overall, this project has provided a detailed, holistic and integrated understanding of sex chromosomes and the genetic architecture of sex-specific phenotypes.
