Abstract
Snakes exhibit genetic sex determination, with female heterogametic sex chromosomes (ZZ males, ZW females). Extensive cytogenetic work has suggested that the level of sex chromosome heteromorphism varies among species, with Boidae having entirely homomorphic sex chromosomes, Viperidae having completely heteromorphic sex chromosomes, and Colubridae showing partial differentiation. Here, we take a genomic approach to compare sex chromosome differentiation in these three snake families. We identify homomorphic sex chromosomes in boas (Boidae), but completely heteromorphic sex chromosomes in both garter snakes (Colubridae) and pygmy rattlesnake (Viperidae). Detection of W-linked gametologs enables us to establish the presence of evolutionary strata on garter and pygmy rattlesnake sex chromosomes where recombination was abolished at different time points. Sequence analysis shows that all strata are shared between pygmy rattlesnake and garter snake, i.e., recombination was abolished between the sex chromosomes before the two lineages diverged. The sex-biased transmission of the Z and its hemizygosity in females can impact patterns of molecular evolution, and we show that rates of evolution for Z-linked genes are increased relative to their pseudoautosomal homologs, both at synonymous and amino acid sites (even after controlling for mutational biases). This demonstrates that mutation rates are male-biased in snakes (male-driven evolution), but also supports faster-Z evolution due to differential selective effects on the Z. Finally, we perform a transcriptome analysis in boa and pygmy rattlesnake to establish baseline levels of sex-biased expression in homomorphic sex chromosomes, and show that heteromorphic ZW chromosomes in rattlesnakes lack chromosome-wide dosage compensation. Our study provides the first full scale overview of the evolution of snake sex chromosomes at the genomic level, thus greatly expanding our knowledge of reptilian and vertebrate sex chromosomes evolution.
Highlights
Heteromorphic sex chromosomes are derived from ordinary autosomes [1,2]
We sequence the genomes of three snake species that display varying levels of sex chromosome heteromorphism and perform a comparative genome analysis
Genome and Transcriptome Assemblies in Snakes We sequenced the genome of a single male and single female of the common garter snake (T. elegans, family Colubridae) and pygmy rattlesnake (S. miliarius, family Viperidae), as well as a single female boa (B. constrictor, family Boidae; publically available male boa reads and scaffolds were obtained from the Assemblathon website, see Methods)
Summary
Heteromorphic sex chromosomes are derived from ordinary autosomes [1,2]. The acquisition of a sex-determining gene initiates sex chromosome evolution, and in many lineages, initially identical homomorphic sex chromosomes differentiated into heteromorphic sex chromosomes [1,2]. Differentiation of homomorphic sex chromosomes resulting in heteromorphic sex chromosomes is a byproduct of degeneration of non-recombining regions along the Y or W chromosome, and can encompass the entire chromosome, or just parts of it. Why some species abolish recombination along their sex chromosomes and acquire heteromorphic XY or ZW chromosomes, while others maintain homomorphic sex chromosomes, is not entirely clear. In principle, this could be due to a lack of sexually antagonistic mutations in some species, or the resolution of conflict imposed by sexually antagonistic mutations by evolving sex-specific or sex-biased expression [5]
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