Avian Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and W Degeneration

Abstract

How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (Myr) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Myr ago formed “neo-sex chromosomes” consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and while the added-Z has remained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that recombination between the homologous added-Z and -W regions continued after the fusion event, and that recombination suppression across this region took several million years to be completed. Moreover, recombination suppression was initiated across multiple positions over the added-Z, which is not consistent with a simple linear progression starting from the fusion point. As expected following recombination suppression, the added-W show signs of degeneration including repeat accumulation and gene loss. Finally, we present evidence for non-random maintenance of slowly evolving and dosage-sensitive genes on both ancestral- and added-W, a process causing correlated evolution among orthologous genes across broad taxonomic groups, regardless of sex-linkage.

Neo‐sex chromosome evolution and phenotypic differentiation across an elevational gradient in horned larks (Eremophila alpestris)

“…The presence of large neo‐sex chromosomes in Horned Larks has previously been reported (De et al, 2010; Bulatova, 1973; Dierickx et al, 2020; Sigeman et al, 2019), but the exact nature and compositions of these fusions was heretofore unknown (but see Sigeman et al, 2021). At least three chromosomes have signals of translocation, corresponding to Zebra Finch chromosomes 3, 4A, and 5 (Figure ; Dierickx et al, 2020; Sigeman et al, 2019).…”

“…The analysis of genomic coverage supports this idea as the coverage of the regions are between those of pure Z chromosome scaffolds and regular autosomal scaffolds (Figure ). Independent translocations to both the Z and W chromosomes or integration of fused elements of Z chromosome pseudoautosomal regions (PARs) to the W chromosome (Sigeman et al, 2019, 2021) would allow these regions to subsequently diverge, since there is little recombination between the Z and W chromosomes. This interpretation is further supported by karyotypic data from Horned Larks and other lark species that show enlargement of both the Z and W chromosomes (Bulatova, 1973).…”

SexFindR: A computational workflow to identify young and old sex chromosomes

“…This approach is often used successfully with genomic data from only a single male and single female to identify heteromorphic sex chromosomes (Palmer et al 2019). Large-scale coverage differences have been used to identify sex chromosomes in a range of species, including insects (Vicoso and Bachtrog 2015), reptiles (Vicoso et al 2013), birds (Sigeman, Strandh, et al 2021), and plants (Müller et al 2020).…”

ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp

“…females are ZW, males are ZZ) have remained relatively understudied, as they are not found in any of the main model organisms. While parallels exist between the evolution of XY and ZW pairs, such as 4 the progressive loss of recombination and subsequent degradation of the Y/W-chromosomes (Ellegren 2011;Vicoso et al 2013;Zhou et al 2014;Picard et al 2018;Sigeman et al 2021), some aspects of their evolution seem to differ. In particular, dosage compensation of Zchromosomes is often limited to a few dosage-sensitive genes (i.e.…”