A bird’s white-eye view on avian sex chromosome evolution

Abstract

Chromosomal organization is relatively stable among avian species, especially with regards to sex chromosomes. Members of the large Sylvioidea clade however have a pair of neo-sex chromosomes which is unique to this clade and originate from a parallel translocation of a region of the ancestral 4A chromosome on both W and Z chromosomes. Here, we took advantage of this unusual event to study the early stages of sex chromosome evolution. To do so, we sequenced a female (ZW) of two Sylvioidea species, a Zosterops borbonicus and a Z. pallidus. Then, we organized the Z. borbonicus scaffolds along chromosomes and annotated genes. Molecular phylogenetic dating under various methods and calibration sets confidently confirmed the recent diversification of the genus Zosterops (1-3.5 million years ago), thus representing one of the most exceptional rates of diversification among vertebrates. We then combined genomic coverage comparisons of five males and seven females, and homology with the zebra finch genome (Taeniopygia guttata) to identify sex chromosome scaffolds, as well as the candidate chromosome breakpoints for the two translocation events. We observed reduced levels of within-species diversity in both translocated regions and, as expected, even more so on the neoW chromosome. In order to compare the rates of molecular evolution in genomic regions of the autosomal-to-sex transitions, we then estimated the ratios of non-synonymous to synonymous polymorphisms (N/S) and substitutions (dN/dS). Based on both ratios, no or little contrast between autosomal and Z genes was observed, thus representing a very different outcome than the higher ratios observed at the neoW genes. In addition, we report significant changes in base composition content for translocated regions on the W and Z chromosomes and a large accumulation of transposable elements (TE) on the newly W region. Our results revealed contrasted signals of molecular evolution changes associated to these autosome-to-sex transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak support for a fast-Z effect.

Extreme variation in recombination rate and genetic diversity along the Sylvioidea neo‐sex chromosome

“…A recent study on white‐eyes ( Zosterops spp. ), another Sylvioidea genus that shares the same neo‐sex chromosome system as the great reed warbler, also found that added‐Z genes and autosomal genes had similar dN/dS values despite the lower recombination rate on chromosome Z (as inferred from low GC content, Leroy et al, 2021). Further, a neo‐sex chromosome in monarch butterfly ( Danaus plexippus ) showed evolutionary rate variation depending on both the age of sex‐linkage (added‐ and ancestral‐Z regions) and the gene expression pattern, highlighting the role of other factors in addition to recombination affecting these rates (Mongue et al, 2021).…”

A novel neo‐sex chromosome in Sylvietta brachyura (Macrosphenidae) adds to the extraordinary avian sex chromosome diversity among Sylvioidea songbirds

“…Previous work on several other Sylvioidea species has, however, already confirmed that the 9.6 Mb-end of the translocated part of chromosome 4A has fused to the 72.9 Mb-end of chromosome Z (i.e. Z 0-72.9(+) -4A 9.6-0(−) ; Leroy et al, 2021;Sigeman et al, 2021) and that the remaining part of chromosome 4A segregates as an independent autosome (Ponnikas et al, 2022). Therefore, we assume that this is also the situation in Sylvietta.…”

“…The avian ZW sex chromosome system was long viewed as extremely stable (Nanda et al, 2008). However, recent discoveries of neo-sex chromosomes have revealed that avian sex chromosomes are more variable than was previously believed (Burley et al, 2022;Dierickx et al, 2020;Gan et al, 2019;Huang et al, 2021;Kretschmer et al, 2020;Leroy et al, 2021;Pala, Naurin, et al, 2012;Sardell, 2016;Sigeman et al, 2019Sigeman et al, , 2020. The most diverse avian sex chromosomes currently known are found among members of the Sylvioidea (Dierickx et al, 2020;Leroy et al, 2021;Sigeman et al, 2019Sigeman et al, , 2020.…”

Varied diversification patterns and distinct demographic trajectories in Ethiopian montane forest bird (Aves: Passeriformes) populations separated by the Great Rift Valley

“…However, there were a few outlier regions for both statistics; first, F ST estimates were slightly higher on the Z chromosome, and second, part of the 4A chromosome shows elevated values of D XY in both the Abyssinian Catbird and the Ethiopian White‐eye. These increased relative values of D XY in these two taxa are expected, as part of the Zebra Finch chromosome 4A has been shown to be part of a neo‐sex chromosome region in the Sylvioidea clade (Leroy et al, 2019) sensu Oliveros et al (2019). We may expect higher genetic differentiation on sex chromosomes due to their lower relative effective population size compared to autosomes and the propensity for sex chromosomes to accumulate structural variants (e.g., Hooper et al, 2018).…”