Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks

Abstract

Given that the genome of males and females are almost identical with the exception of genes on the Y (or W) chromosome or sex-determining alleles (in organisms without sex chromosomes), it is likely that many downstream processes resulting in sexual dimorphism are produced by changes in regulation. In early stages of sex chromosome evolution, as the Y-chromosome degenerates, gene expression should be significantly impacted for genes residing on the sex chromosome pair as regulatory mutations accumulate. However, this has rarely been examined because most model organisms have clearly diverged sex chromosomes. Fish provide a unique opportunity to examine the evolution of sex chromosomes because genetic sex determination has evolved quite recently in some groups of fish. We compared sex-specific transcription in threespine stickleback (Gasterosteus aculeatus) liver tissue using a long-oligo microarray. Of the 1,268 genes that were differentially expressed between sexes, a highly significant proportion (23%) was concentrated on chromosome 19, corresponding to the recently described nascent sex chromosomes. The sex-biased genes are enriched for different functional categories in males and females, although there is no specific functional enrichment on the sex chromosomes. Female-biased genes are concentrated at one end of the sex chromosome, corresponding to a deletion in the Y, suggesting a lack of global dosage compensation. Prior research on threespine sticklebacks has demonstrated various degrees of dissimilarity in upstream regions of genes on the Y providing a potential mechanism for the observed patterns of female-biased expression. We hypothesize that degeneration of the Y chromosome results in regulatory mutations that create a sex-specific expression pattern and that this physical concentration of sex-biased expression on the nascent sex chromosome may be a key feature characterizing intermediate phases of sex chromosome evolution.