Abstract
Standard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large nondegenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over >100 Myr, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analyzed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in differentiated regions for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species, PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.
Highlights
Sex chromosomes are thought to evolve from autosomes that acquire a sex determination locus (Bull 1983)
In the differentiated regions (DRs), reads arising from the W in females will not map to the homologous region of the Z, whereas in the pseudoautosomal regions (PARs), reads from both the Z and the W will map to the Z chromosome
We expect coverage of sequencing reads mapped to the Z chromosome in the DR to be 1⁄2 that of the autosomes or PAR in females, logically similar to the approach used to annotate Y and W chromosomes in other species (Chen et al 2012; Carvalho and Clark 2013; Tomaszkiewicz et al 2017)
Summary
Sex chromosomes are thought to evolve from autosomes that acquire a sex determination locus (Bull 1983). Recombination suppression leads to the formation of evolutionary strata, which can occur multiple times in the course of sex chromosome evolution (Lahn and Page 1999; Bergero and Charlesworth 2009; Cortez et al 2014; Zhou et al 2014; Wright et al 2016; Xu et al 2019) Despite differences in their autosomal origins and heterogamety, eutherian mammals and neognathous birds followed similar but independent trajectories of sex chromosome evolution (Graves 2015; Bellott et al 2017). In some species of frogs, homomorphic sex chromosomes appear to be maintained by occasional XY recombination in sex-reversed XY females (the ‘fountain of youth’ model), which is possible if recombination suppression is independent of genotype and instead a consequence of phenotypic sex, such that XY females experience normal recombination (Perrin 2009; Dufresnes et al 2015; Rodrigues et al 2018)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
