Complex evolutionary trajectories of sex chromosomes across bird taxa

Abstract

Sex-specific chromosomes, like the W of most female birds and the Y of male mammals, usually have lost most genes owing to a lack of recombination. We analyze newly available genomes of 17 bird species representing the avian phylogenetic range, and find that more than half of them do not have as fully degenerated W chromosomes as that of chicken. We show that avian sex chromosomes harbor tremendous diversity among species in their composition of pseudoautosomal regions and degree of Z/W differentiation. Punctuated events of shared or lineage-specific recombination suppression have produced a gradient of “evolutionary strata” along the Z chromosome, which initiates from the putative avian sex-determining gene DMRT1 and ends at the pseudoautosomal region. W-linked genes are subject to ongoing functional decay after recombination was suppressed, and the tempo of degeneration slows down in older strata. Overall, we unveil a complex history of avian sex chromosome evolution.

Evolutionary stability of sex chromosomes in snakes

“…In conclusion, advanced snakes have highly evolutionarily stable sex chromosomes comparable with iguanas, viviparous mammals and birds [5,31,32]. This supports the hypothesis of the stability of GSD when compared with ESD ('GSD as an evolutionary trap' hypothesis), although ESD might be ancestral for squamates, and maybe all amniotic vertebrates [1,2,3].…”

Mammalian X homolog acts as sex chromosome in lacertid lizards

“…Degenerated W or Y chromosomes lack in the non-recombining region that most of the genes present on their Z or X counterparts, respectively (see, for example. Rovatsos et al, 2014cRovatsos et al, , 2015Zhou et al, 2014). Therefore, we can assume that the female gene pool in TSE should contain just a single allele for all single-copy Z-specific loci because they are hemizygous in this sex.…”

“…As far as we know, sex chromosomes of lacertids are not homologous with those of other sauropsid lineages with known gene content, such as advanced snakes (Matsubara et al, 2006;Vicoso et al, 2013), iguanas (see, for example, Alföldi et al, 2011;Rovatsos et al, 2014a-c), geckos (Kawai et al, 2009), turtles (see, for example, Kawagoshi et al, 2012Kawagoshi et al, , 2014 and birds (see, for example, Zhou et al, 2014). The lacertid Z chromosome partially shares gene content with the ancestral therian X, and thus we assume that these sex chromosome systems probably evolved from the same ancestral chromosome (syntenic block).…”

“…In any case, more robust testing of the hypotheses of the ancestral sex determination and on the evolution of sex-determining mechanisms in amniotes is largely precluded by our very limited knowledge about the homology of sex chromosomes and sex-determining genes among particular groups. The homology of sex chromosomes can be inferred from the knowledge of the gene content of sex chromosomes; however, it has been identified in only a few amniote lineages such as viviparous mammals (see, for example, Kohn et al, 2004) and monotremes (see, for example, Rens et al, 2007), birds (see, for example, Zhou et al, 2014), several turtle species (see, for example, Kawagoshi et al, 2012Kawagoshi et al, , 2014, advanced snakes (Matsubara et al, 2006;Vicoso et al, 2013;Rovatsos et al, 2015), iguanas (see, for example, Alföldi et al, 2011;Rovatsos et al, 2014a-c), a gecko (Kawai et al, 2009) and recently also a lacertid lizard (Srikulnath et al, 2014).…”

Avian transcriptomics: opportunities and challenges

“…In contrast to mammals, birds have evolved a female heterogametic sex system, with females having two distinct sex chromosomes (ZW) and males two copies of the Z chromosome (ZZ) (Ellegren 2000). The distinct pattern of inheritance in sex chromosomes means that they experience evolutionary forces different from the rest of the genome (Mank et al 2010), and they have hence been subject to a number of evolutionary studies in birds (Wang et al 2014;Zhou et al 2014), also using transcriptomic data (Balakrishnan et al 2013;Künstner et al 2010;Ramstad et al 2016;Wright et al 2015). Wright et al (2015) studied sequence and expression data of sex chromosomes simultaneously in six species of birds using RNA-seq data.…”