Analysis of Sex Chromosome Evolution in the Clade Palaeognathae from Phased Genome Assembly

Abstract

Birds in the clade Palaeognathae, excluding Tinamiformes, have morphologically conserved karyotypes and less differentiated ZW sex chromosomes compared with those of other birds. In particular, the sex chromosomes of the ostrich and emu have exceptionally large recombining pseudoautosomal regions (PARs), whereas non-PARs are classified into two strata according to the date of their origins: stratum 0 and stratum 1 (S1). However, the construction and analysis of the genome sequences in these regions in the clade Palaeognathae can be challenging because assembling the S1 region is difficult owing to low sequence diversity between gametologs (Z-linked and W-linked sequences). We addressed this issue by applying the Platanus-allee assembler and successfully constructed the haplotype-resolved (phased) assembly for female emu, cassowary, and ostrich using only sequence read data derived from the Illumina platform. Comparative genomic and phylogenetic analyses based on assembled Z-linked and W-linked sequences confirmed that the S1 region of emu and cassowary formed in their common ancestor. Moreover, the interspersed repetitive sequence landscapes in the S1 regions of female emu showed an expansion of younger repetitive elements in the W-linked S1 region, suggesting an interruption in homologous recombination in the S1 region. These results provide novel insights into the trajectory of sex chromosome evolution in the clade Palaeognathae and suggest that the Illumina-based phased assembly method is an effective approach for elucidating the evolutionary process underlying the transition from homomorphic to differentiated sex chromosomes.

Sex chromosome cycle as a mechanism of stable sex determination

“…Indeed, most sex chromosomes that emerged more than 100 Mya are fully differentiated, with extensive gene loss on the Y and W. Mammalian Ys and avian Ws are typical examples of degenerated sex chromosomes ( 77 ) . Although species in Palaeognathae, such as emu, are exceptions ( 31 , 78 ) , many mammals and birds have lost a majority of genes on the Y and W, respectively. In species with a degenerated Y and W, the functions of these chromosomes have become specialized for sex determination.…”

Avian Introgression Patterns are Consistent With Haldane’s Rule

“…Although these patterns are consistent with Haldane’s Rule, they could also be explained by the higher mutation rates in mtDNA ( Ballard and Whitlock 2004 ) or selective sweeps on autosomal loci ( Hejase et al 2020 ). In addition, methodological issues in assembling sex chromosomes from genomic data—which often have lower coverage—might result in biased estimates of genetic differentiation and consequent inferences of introgression rates ( Okuno et al 2021 ). Based on these theoretical and methodological uncertainties, I decided to omit studies that infer introgression patterns from genetic divergence, resulting in the removal of several genomic studies from the literature search.…”

The Length Polymorphism of the 9th Intron in the Avian CHD1 Gene Allows Sex Determination in Some Species of Palaeognathae

“…It is believed that regional suppression of recombination of a pair of autosomes led evolutionarily to the formation of the bird Z and W chromosomes [ 17 , 18 ]. Neognathous birds have significantly differentiated sex chromosomes with usually a smaller, degenerate, low gene content and highly heterochromatized W chromosome, whereas in palaeognathous birds, the Z and W chromosomes are often homomorphic or little differentiated with exceptionally large recombining pseudoautosomal regions [ 17 , 19 , 20 ]. The most basal forms of avian sex chromosomes recombine along most of their length occur in ratites, whereas in tinamous, signs of intermediate Z–W differentiation can be observed [ 21 , 22 ].…”