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

Abstract

Sex chromosomes diverge after the establishment of recombination suppression, resulting in differential sex-linkage of genes involved in genetic sex determination and dimorphic traits. This process produces systems of male or female heterogamety wherein the Y and W chromosomes are only present in one sex and are often highly degenerated. Sex-limited chromosomes (e.g., Y and W) contain valuable information about the evolutionary transition from autosomes to sex chromosomes, yet detailed characterizations of the structure, composition, and gene content of sex-limited chromosomes is lacking for many species. In this study, we characterize the female-specific W chromosome of the prairie rattlesnake (Crotalus viridis) and evaluate how recombination suppression and other processes have shaped sex chromosome evolution in ZW snakes. Our analyses indicate that the rattlesnake W chromosome is over 80% repetitive and that an abundance of GC-rich mdg4 elements has driven an overall high degree of GC-richness despite a lack of recombination. The W chromosome is also highly enriched for repeat sequences derived from endogenous retroviruses and likely acts as a ‘refugium’ for these and other retroelements. We annotated 219 putatively functional W-linked genes across at least two evolutionary strata identified based on estimates of sequence divergence between Z and W gametologs. The youngest of these strata is relatively gene-rich, however gene expression across strata suggests retained gene function amidst a greater degree of degeneration following ancient recombination suppression. Functional annotation of W-linked genes indicates a specialization of the W chromosome for reproductive and developmental function since recombination suppression from the Z chromosome.

The State of Squamate Genomics: Past, Present, and Future of Genome Research in the Most Speciose Terrestrial Vertebrate Order

“…The developmental and evolutionary basis for various forms of sex determination across vertebrates is an active area of research, with direct implications to issues of climate change and conservation [164]. Squamate diversity possesses the three main forms of sex determination systems: genotypic sex determination with female heterogamety (ZZ/ZW; [165,166]), male heterogamety (XX/XY; [167]), and temperature dependence [168]). Some species have mixed systems with both genotypic and environmental sex determination, such as the snow skink (Niveoscincus ocellatus), which transitions to a temperature-dependent system in certain climates [169].…”

Has recombination changed during the recent evolution of the guppy Y chromosome?

“…The large regions in which crossovers are infrequent in the male maps are at the start of the assembly for 17 of the 23 guppy chromosomes, whereas GC content in introns and third codon positions is high at the opposite ends, suggesting that this reflects very high recombination rates in males, due to GC-biased gene conversion (Charlesworth et al 2020b). To exclude the possibility that this pattern might instead reflect preferential presence of GC-rich transposable element(s) near the chromosome termini (Schield et al 2022), we repeated the GC content analyses after masking repetitive sequences, and also identified a likely centromeric satellite sequence (see the Methods section). These analyses confirmed the centromeric ends previously identified (Supplementary Figures S2 and S3) and identified their positions near one end of each chromosome (Supplementary Table S2).…”