Positive selection drivescis-regulatory evolution across the threespine stickleback Y chromosome

Abstract

AbstractAllele-specific gene expression evolves rapidly across gametologs on heteromorphic sex chromosomes (X and Y or Z and W). Current models of sex chromosome evolution suggest this occurs through the rapid accumulation of mutations within regulatory regions. However, these patterns have not been demonstrated empirically due to the limited number of Y chromosome assemblies available to survey sequence evolution outside of coding regions. The threespine stickleback (Gasterosteus aculeatus) Y chromosome is an ideal model to test hypotheses of rapid regulatory evolution due to its intermediate state of divergence from the X chromosome. A large number of Y-linked gametologs still exist across three differently aged evolutionary strata to test these hypotheses. We found that putative enhancer regions (accessible chromatin regions defined through ATAC-seq) on the Y chromosome exhibited elevated substitution rates when compared to intergenic regions and synonymous sites within coding regions. This strongly suggests that many regulatory regions are under positive selection on the Y chromosome. This divergence was correlated with X-biased gametolog expression, indicating the loss of expression from the Y chromosome may be favored by selection. Our findings provide evidence that Y-linked regulatory regions exhibit signs of positive selection quickly after the suppression of recombination, supporting recent theoretical models that show the rapid divergence of regulatory regions may be favored to mask deleterious mutations on the Y chromosome.