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Association of Sly with sex-linked gene amplification during mouse evolution: a side effect of genomic conflict in spermatids?

In common with other mammalian sex chromosomes, the mouse sex chromosomes are enriched for genes with male-specific function such as testis genes. However, in mouse there has been an unprecedented expansion of ampliconic sequence containing spermatid-expressed genes. We show via a phylogenetic analysis of gene amplification on the mouse sex chromosomes that multiple families of sex-linked spermatid-expressed genes are highly amplified in Mus musculus subspecies and in two further species from the Palaearctic clade of mouse species. Ampliconic X-linked genes expressed in other cell types showed a different evolutionary trajectory, without the distinctive simultaneous amplification seen in spermatid-expressed genes. The Palaearctic gene amplification occurred concurrently with the appearance of Sly, a Yq-linked regulator of post-meiotic sex chromatin (PMSC) which acts to repress sex chromosome transcription in spermatids. Despite the gene amplification, there was comparatively little effect on transcript abundance, suggesting that the genes in question became amplified in order to overcome Sly-mediated transcriptional repression and maintain steady expression levels in spermatids. Together with the known sex-ratio effects of Yq/Sly deficiency, our results suggest that Sly is involved in a genomic conflict with one or more X-linked sex-ratio distorter genes. The recent evolution of the novel PMSC regulator Sly in mouse lineages has significant implications for the use of mouse-model systems in investigating sex chromosome dynamics in spermatids.