Evolution and expression patterns of the neo-sex chromosomes of the crested ibis

Abstract

Bird sex chromosomes play a unique role in sex-determination, and affect the sexual morphology and behavior of bird species. Core waterbirds, a major clade of birds, share the common characteristics of being sexually monomorphic and having lower levels of inter-sexual conflict, yet their sex chromosome evolution remains poorly understood. Here, by we analyse of a chromosome-level assembly of a female crested ibis (Nipponia nippon), a typical core waterbird. We identify neo-sex chromosomes resulting from fusion of microchromosomes with ancient sex chromosomes. These fusion events likely occurred following the divergence of Threskiornithidae and Ardeidae. The neo-W chromosome of the crested ibis exhibits the characteristics of slow degradation, which is reflected in its retention of abundant gametologous genes. Neo-W chromosome genes display an apparent ovary-biased gene expression, which is largely driven by genes that are retained on the crested ibis W chromosome but lost in other bird species. These results provide new insights into the evolutionary history and expression patterns for the sex chromosomes of bird species.

The rate of W chromosome degeneration across multiple avian neo-sex chromosomes

“…In those lineages, we estimated that on average 3.4 genes were lost per million years across lineages, corresponding to 1.0% gene loss per million years when accounting for the variation in the number of genes at the time of strata formation of each lineage (Table 1 ). This rate of gene loss is lower than on the neo-sex chromosome found among parrots, where only 16.9% of the genes remain on the added part after 31.8 Myr of evolution (corresponding to a 2.6% gene loss/Myr; 20 ), but higher than that of the neo-sex chromosome in the crested ibis, where only 20% were lost 24 after ~ 53 Myr ( 62 ; age according to strata S3), corresponding to a gene loss rate of 0.4 genes/Myr. Our study is based on short-read data whereas the parrot and ibis studies utilize data from assembled genomes 20 , 24 .…”

“…This rate of gene loss is lower than on the neo-sex chromosome found among parrots, where only 16.9% of the genes remain on the added part after 31.8 Myr of evolution (corresponding to a 2.6% gene loss/Myr; 20 ), but higher than that of the neo-sex chromosome in the crested ibis, where only 20% were lost 24 after ~ 53 Myr ( 62 ; age according to strata S3), corresponding to a gene loss rate of 0.4 genes/Myr. Our study is based on short-read data whereas the parrot and ibis studies utilize data from assembled genomes 20 , 24 . A potential risk of using short-read data is incorrect assignment of SNPs as W-linked when they actually represent Z polymorphisms, thereby overestimating the rate of W degeneration.…”

“…The sex chromosomes of birds, which formed > 100 million years ago (Mya), were previously thought to be extremely stable and share the same gene content across the entire clade 16 , 17 . Recently, however, this notion has been challenged with neo-sex chromosomes being found in several lineages 18 , including in parrots, cuckoos, crested ibis, and songbirds 19 – 24 .…”