Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

Abstract

Sex chromosomes of mammals and most birds are heteromorphic, while those of many paleognaths (ratites and tinamous) are inexplicably homomorphic. To dissect the mechanisms underlying the different tempo of sex chromosome evolution, we produced high-quality genomes of 12 paleognathous species, and reconstructed their phylogeny based on alignments of the non-coding sequences extending to nearly 40% of the genome. Our phylogenomic tree grouped the South American rheas and tinamous together, and supported the independent evolution of gigantism and loss of flight among ratites. The small-bodied tinamous have much higher rates of genome-wide substitutions and transposon turnovers. Yet majorities of both have retained exceptionally long recombining regions occupying over half of the entire sex chromosome, with the rest sex-linked regions diverging from each other at a much lower rate relative to neognathous birds. Each species exhibits a punctuated sequence divergence pattern between sex chromosomes termed 'evolutionary strata', because of stepwise suppression of recombination. We concluded that all paleognaths share one evolutionary stratum with all other birds, and convergently formed between one to three strata after their rapid speciation. Contrary to the classic notion, we provided clear evidence that the youngest stratum of some tinamous formed without chromosomal inversion. Intriguingly, some of the encompassing W-linked genes have upregulated their expression levels in ovary, probably due to the female-specific selection.We proposed here that the unique male-only parental care system of paleognaths has reduced the intensity of sexual selection, and contributed to these species' low rates of sex chromosome evolution. We also provided novel insights into the evolution of W-linked genes at their early stages.

The Female-Specific W Chromosomes of Birds Have Conserved Gene Contents but Are Not Feminized

“…The more complete datasets of the W-linked sequences and genes of the S0 made it possible for us to better examine the conservation level of the W-linked S0 region that was previously considered highly degenerated across all birds. On the other hand, the independently evolved S1 of paleognaths and neognaths [ 7 , 35 , 40 ] is a useful model to identify common evolutionary forces that convergently shape the gene content of the avian W chromosomes.…”

“…The genomes and gametologous sequences of songbirds and chicken were directly retrieved from [ 8 ] and [ 39 ]. We re-analyzed the genomes of tinamous and ratites that were published in [ 40 ] and [ 35 ] using the same pipeline as in Xu el al. [ 8 ].…”

“…We searched the homologous sex chromosome sequences in the newly assembled female genomes in Wang et al [ 40 ] with a different pipeline used in Xu et al [ 8 ]. To reduce both false positives and false negatives in the homologous searches, we chose the available Z chromosome sequence of most closely related species as a reference, rather than using the basal ostrich which is quite divergent from other paleognaths.…”

“…When more than 60% of the sequence of a scaffold was aligned with reference Z chromosome, the scaffold was assigned as sex-chromosome linked. This threshold is different from the 50% of aligned sequences with at least 1 kb long, and sequence similarity between 70% and 95% used in [ 40 ].…”

“…To elucidate the evolutionary forces that impact the evolution of avian sex chromosomes, we collected the published female genomes from 11 songbirds [ 8 ] of Neoaves, one Galloanserae (chicken) [ 39 ], five ratites, and 10 tinamous [ 35 , 40 ] of Palaeognathae species that span the three major clades of birds. Particularly, we applied our analytical pipeline [ 8 ] to re-analyze the genomic data of Palaeognathae [ 40 ]. The comparative study of the sex-linked sequences from those species, combined with gene expression data from multiple tissues of both sexes, allows for a systematic assessment for the signature of W chromosome feminization.…”