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Recombination, sex-specific adaptation and evolution of the poeciliid sex chromosomes

Periodic Reporting for period 3 - GuppY (Recombination, sex-specific adaptation and evolution of the poeciliid sex chromosomes)

Reporting period: 2019-08-01 to 2021-01-31

Sex chromosomes have evolved independently countless times throughout the eukaryotes. As such, sex chromosomes represent one of the most pervasive examples of convergent evolution, as analogous yet unrelated sex chromosomes share many unique features that distinguish them from the rest of the genome. Although models for sex chromosome evolution have been proposed, they have been difficult to empirically test, largely because most model systems are at a terminal phase of sex chromosome divergence. Most work on sex chromosomes has therefore focused on the consequences of sex chromosome evolution, rather than the causes. In order to understand the forces catalyzing sex chromosome evolution, we require a study system at earlier stages of sex chromosome divergence, ideally one where there is still extensive polymorphism among populations and closely related species in the degree and region of recombination suppression, and with easily identified sexually antagonistic traits. These traits are all exhibited by the Poeciliid fishes, the focus of GuppY, which is designed to test long-standing theories about sex chromosome evolution. The overarching goals of the project are to identify the mechanisms, catalysts and consequences of recombination suppression between the sex chromosomes, and then to quantify the role of sex-specific selection and sexual conflict in sex chromosome evolution and subsequent divergence. These goals will be accomplished through the synthesis of comparative, phenotypic and next-generation molecular genetic approaches in order to provide a cohesive and multi-faceted understanding of sex chromosome evolution. Moreover, these goals will be performed across three evolutionary levels, integrating patterns of variation within populations, among populations, and across related species, encompassing short, medium and long time-spans and yielding unprecedented insight into multiple stages of evolutionary history. More broadly, this work will provide fundamental insights into the evolutionary processes within species, and how the genome responds to conflicting selection pressures. T
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 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 work is available in pre-print form (Darolti et al. Biorxiv 2019) and is currently in review.
In this project, we are developing new bioinformatic tools to deal with both sequence and phenotypic data. We expect our final results to provide unique insight into the evolution of male and female phenotypes, and the mechanisms by which the Y chromosome evolves.
Guppies, credit Clara Lacy