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.

Fig. 1. Evolutionary strata of avian sex chromosomes

Fig. 2. Emergence of evolutionary strata in different avian lineages

Shown are Venn diagrams of overlapping gene content between orthologous strata of different Palaeognathae (A to C) and Neognathae (D to F) species. To the right of each diagram is a maximum-likelihood tree for a specific example gene constructed from Z- and W-linked gametologs of that stratum. Additional trees supporting the inference of a certain stratum’s age are shown in the figs. S12, S14, S16, and S17. The tree is constructed with ostrich or green anole lizard as outgroup, with 100 bootstraps. A pattern in which Z gametologs are grouped together by species indicates that Z/W recombination was suppressed before their speciation, whereas clustering of Z and W gametologs of the same species indicates that Z/W recombination was suppressed after the speciation event. “Palaeognathae PAR” shows the number of genes that overlapped between ostrich PAR, emu PAR, and tinamou stratum S2. “Neoaves S3” shows the overlapped gene content between tropicbird PAR versus S3 of four other Neoaves species: killdeer, brown mesite, crested ibis, and barn owl.

Fig. 3. Gene synteny within avian evolutionary strata

Mapped is the evolutionary strata gene synteny between sequenced reptile (boa and lizard) and avian species. Each line connects a pair of orthologous genes between species, and different colors of lines represent different strata of genes: S0 (gray), ostrich S1 (yellow), Neognathae S1 (brown), Neoaves S2 (orange), DMRT1 (red). Genomic regions encompassing S0 and S1 have experienced multiple inversions across different species, relocating DMRT1 to the middle of the Z chromosome after the divergence between Neognathae and Palaeognathae. In contrast, genomic regions within Neoaves S2 and S3 show high level of syntenic conservation across species.

Fig. 4. Evolution of avian W-linked genes

(A to G) For each stratum of the example species, we show a pie chart of gene composition on the W with regards to whether their open reading frames (ORFs) are predicted to be intact or not. The x axis is the estimated age, and y axis is the Z/W divergence level of each stratum. Within each pie chart, we show W-linked genes that cannot be found within the assembled sequences (gray), genes with disrupted ORFs that contain premature stop codons or frameshift mutations (blue), and genes with intact ORFs (red). Note that the number of missing genes may be overestimated, owing to the difficulty of assembling W-linked genes surrounded by repetitive sequences. (H) Comparison of gene expression between Z and W linked gametologs in ostrich brain and liver samples, relative to their autosomal lizard orthologs. We show significance level of Wilcoxon test comparing the gametolog expression versus that of lizard (**P < 0.01). W gametologs show a significant down-regulation of gene expression. (I) Correlation between gene loss rate and age of stratum. Each data point represents a stratum of a certain bird species (dot) in Fig. 1 or human (triangle). The data for the human Y chromosome are derived from (49, 51).

Fig. 5. Hypothesized formation scenarios of avian evolutionary strata

We designate DMRT1 on the chromosome with the red bar, and homologous recombination between proto–sex chromosomes at PAR (in green) with intersecting lines. Gray or black regions on the W chromosome represent the female-specific region lacking recombination, with darker color representing higher level of differentiation between Z/W. We also show inferred Z- or W-linked inversions that have led to the formation of certain evolutionary strata on the tree.