Evolutionary analysis of the female-specific avian W chromosome

Abstract

The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear–cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.

How to identify sex chromosomes and their turnover

“…This is because heteromorphic sex chromosomes still retain sequence orthology between the X and Y, and incorrectly mapped reads can mask coverage differences between the sexes and lead to the misclassification of sex‐linked sequences as autosomal. Stringent mapping parameters are recommended to minimize false negatives, with a maximum mismatch of 0 or 1 (Carvalho & Clark, ; Hall et al, ; Smeds et al, ; Vicoso et al, ), as well as the filtering of nonuniquely mapped reads (Vicoso & Bachtrog, ). Furthermore, repetitive regions of DNA should be masked prior to implementing these approaches to remove repeats shared by the sex‐limited chromosome and the autosomes (Carvalho & Clark, ; Hall et al, ; Smeds et al, ; Vicoso & Bachtrog, ).…”

Sex Reversal in Birds

“…The chicken Z chromosome has some 1,000 genes, most of which are unrelated to sex, but there is a bias of sex-related genes on the chicken Z [Bellott et al, 2010]. The chicken W chromosome is a degraded version of the Z, with few bona fide genes, probably around 25-45 [Ayers et al, 2013b;Moghadam et al, 2012;Smeds et al, 2015]. It is noteworthy that DMRT1 is also Z-linked in all other birds, including the ratites (flightless emu, ostrich, etc.…”

“…Advances in chicken transcriptomics and whole chromosome assembly in chicken and other avians have revealed a largely heterochromatic W that harbours perhaps 25-46 genes in the region that does not recombine with the Z and is hence W-specific [Chen et al, 2012;Ayers et al, 2013b;Smeds et al, 2015]. Most of these are highly homologous to copies on the Z (gametologues) with no obvious link to sex [Ayers et al, 2013b;Smeds et al, 2015]. These W genes may be sensitive to dosage and hence are retained as functional partners of their Z gametologues.…”

Direct estimate of the rate of germline mutation in a bird

“…Moreover, alternative means for translating observed sequence divergence into divergence times would act complementary to calibration points based on fossil records for molecular dating in phylogenetic analysis. The collared flycatcher has been subject to detailed genomic investigation, and there is a 1.123-Gb genome assembly with a super-scaffold N50 of 20.2 Mb and with 93.4% of the assembly anchored, ordered, and oriented to chromosomes via a highdensity genetic linkage map (Ellegren et al 2012;Kawakami et al 2014;Smeds et al 2015). Levels of genetic diversity in this species are intermediate to that observed in humans and Drosophila melanogaster, with a mean nucleotide diversity (π) of ≈4 × 10 −3 in different populations .…”