Multi-Copy Gene Family Evolution on the Avian W Chromosome

Abstract

The sex chromosomes often follow unusual evolutionary trajectories. In particular, the sex-limited Y and W chromosomes frequently exhibit a small but unusual gene content in numerous species, where many genes have undergone massive gene amplification. The reasons for this remain elusive with a number of recent studies implicating meiotic drive, sperm competition, genetic drift and gene conversion in the expansion of gene families. However, our understanding is primarily based on Y chromosome studies as few studies have systematically tested for copy number variation on W chromosomes. Here, we conduct a comprehensive investigation into the abundance, variability, and evolution of ampliconic genes on the avian W. First, we quantified gene copy number and variability across the duck W chromosome. We find a limited number of gene families as well as conservation in W-linked gene copy number across duck breeds, indicating that gene amplification may not be such a general feature of sex chromosome evolution as Y studies would initially suggest. Next, we investigate the evolution of HINTW, a prominent ampliconic gene family hypothesized to play a role in female reproduction and oogenesis. In particular, we investigate the factors driving the expansion of HINTW using contrasts between modern chicken and duck breeds selected for different female-specific selection regimes and their wild ancestors. Although we find the potential for selection related to fecundity in explaining small-scale gene amplification of HINTW in the chicken, purifying selection seems to be the dominant mode of evolution in the duck. Together, this challenges the assumption that HINTW is key for female fecundity across the avian phylogeny.

Fourth Report on Chicken Genes and Chromosomes 2022

“…A handful of W-linked multi-copy gene families have been identified in a limited number of avian species [Hori et al, 2000;Backström et al, 2005;Davis et al, 2010;Smeds et al, 2015;Rogers et al, 2021]. The most comprehensively studied of these is histidine triad nucleotidebinding protein (HINTW), an ampliconic gene family that is hypothesized to play a role in female reproduction and oogenesis [O'Neill et al, 2000;Ceplitis and Ellegren, 2004].…”

“…Therefore, HINTW might act to disrupt the function of its Z-linked ortholog (HINTZ) by forming a heterodimer. Interestingly, the size of the HINTW gene family varies between chicken layer breeds subject to artificial selection for fecundity relative to other chicken breeds [Rogers et al, 2021], potentially suggesting a role of female-specific selection in driving gene amplification, although this relationship was absent across duck breeds.…”

The Rattlesnake W Chromosome: A GC-Rich Retroelement Refugium with Retained Gene Function Across Ancient Evolutionary Strata

“…6 D ; supplementary table S3, Supplementary Material online), and 56% of W genes have higher GC3 than the matching Z gametolog. This finding contrasts with the avian W chromosome, for example, which contains few ampliconic genes with higher GC3 than Z gametologs (e.g., HINTW ; Ceplitis and Ellegren 2004 ; Backström et al 2005 ; Smeds et al 2015 ; Rogers et al 2021 ), and suggests that intrachromosomal gene conversion may be comparatively frequent on the snake W chromosome, playing a role in shaping patterns of W-linked synonymous sequence divergence and GC content.…”

“…Using simulations, Marais et al (2010) showed that gene conversion between Y-linked gene copies can be beneficial for opposing Muller’s Ratchet, with greater gene copy number providing an enhanced benefit. Other empirical examples also show a prevalence of gene conversion between amplified gene families on Y and W chromosomes (e.g., Rozen et al 2003 ; Backström et al 2005 ; Connallon and Clark 2010 ; Rogers et al 2021 )—the taxonomically widespread nature of gene conversion on sex-limited chromosomes indeed suggests that it may be advantageous in tempering rates of gene decay. Several lines of evidence support that the counter-degeneration effects of gene conversion are relevant to snake W chromosome evolution.…”

Avian Introgression Patterns are Consistent With Haldane’s Rule

“…The W-chromosome is notoriously difficult to sequence due to its haploid nature and high repeat content ( Tomaszkiewicz et al 2017 ). However, the development of new sequencing technologies for non-model organisms will allow researchers to explore the evolutionary history of this sex chromosome ( Xu et al 2020 ; Rogers et al 2021 ) and its connection to Haldane’s Rule. For example, a recent study reported an excess of endogenous retroviruses (ERVs) on the W-chromosome, which could contribute to genetic incompatibilities between species due to mismatches in ERV-repressor mechanisms in hybrids ( Peona et al 2021 ).…”