Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Abstract

Once recombination is halted between the X and Y chromosomes, 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 the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize 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 roughly 20 million years ago. 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 and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

Conserved ZZ/ZW sex chromosomes in Caribbean croaking geckos (Aristelliger: Sphaerodactylidae)

“…It is thus possible for a sex chromosome pair to have distinct gene content and significant allelic differences even though they appear to be morphologically similar (Conte, Gammerdinger, Bartie, Penman, & Kocher, 2017;Fontaine et al, 2017;Perry et al, 2018;Toups, Rodrigues, Perrin, & Kirkpatrick, 2019;Zhou et al, 2014), including the Aristelliger sex chromosomes presented here. Indeed, there are (Darolti et al, 2019;Kamiya et al, 2012;Kottler et al, 2020;Lahn & Page, 1999;Zhou et al, 2014). Thus, the overly simplistic distinction between homomorphic and heteromorphic sex chromosomes that emerged when cytogenetics was the prevailing technology may fail to describe the continuum of differences between gametologs that can be distinguished using DNA sequence data (Furman et al, 2020).…”

How to identify sex chromosomes and their turnover

“…This is often challenging and highly dependent on conservation of synteny across clades. However, a number of different methods are available for this purpose, including the Reference-Assisted Chromosome Assembly (RACA) algorithm (Kim et al, 2013) as used in Darolti et al (2019), or a custom approach developed by Jeffries et al (2018), involving the generation of linkage maps from RAD-seq data to anchor scaffolds to an outgroup reference genome. The importance of these algorithms, as well as the importance of generating chromosomal-level genome assemblies in multiple species, will be a priority in order to estimate the diversity of sex chromosomes in many undersampled clades.…”

“…Studying species or populations where there is variation in the extent of recombination suppression between sex chromosomes, as in Poeciliids (Bergero et al, 2019;Darolti et al, 2019;, 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, 2018).…”

The Formation of Sex Chromosomes in Silene latifolia and S. dioica Was Accompanied by Multiple Chromosomal Rearrangements

“…As a result of suppressed recombination and accumulation of deleterious mutations, the sex chromosomes differ in their structure, function and gene density. The X chromosome becomes hemizygous and X hemizygosity in males leads to special regulatory mechanisms to equalize the transcription ratio between the X chromosomes and autosomes (Charlesworth and Charlesworth, 2005;Muyle et al, 2017;Darolti et al, 2019). As a result of accumulation of deleterious mutations, the Y chromosome is degenerated and the sex chromosomes may differ even within closely related species as demonstrated in human and chimpanzee (Hughes et al, 2010).…”