Novel Gene Acquisition on Carnivore Y Chromosomes

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Abstract
Despite its importance in harboring genes critical for spermatogenesis and male-specific functions, the Y chromosome has been largely excluded as a priority in recent mammalian genome sequencing projects. Only the human and chimpanzee Y chromosomes have been well characterized at the sequence level. This is primarily due to the presumed low overall gene content and highly repetitive nature of the Y chromosome and the ensuing difficulties using a shotgun sequence approach for assembly. Here we used direct cDNA selection to isolate and evaluate the extent of novel Y chromosome gene acquisition in the genome of the domestic cat, a species from a different mammalian superorder than human, chimpanzee, and mouse (currently being sequenced). We discovered four novel Y chromosome genes that do not have functional copies in the finished human male-specific region of the Y or on other mammalian Y chromosomes explored thus far. Two genes are derived from putative autosomal progenitors, and the other two have X chromosome homologs from different evolutionary strata. All four genes were shown to be multicopy and expressed predominantly or exclusively in testes, suggesting that their duplication and specialization for testis function were selected for because they enhance spermatogenesis. Two of these genes have testis-expressed, Y-borne copies in the dog genome as well. The absence of the four newly described genes on other characterized mammalian Y chromosomes demonstrates the gene novelty on this chromosome between mammalian orders, suggesting it harbors many lineage-specific genes that may go undetected by traditional comparative genomic approaches. Specific plans to identify the male-specific genes encoded in the Y chromosome of mammals should be a priority. Y chromosomes are typically gene poor and enriched with repetitive elements, making them difficult to sequence by standard methods. Hence, the Y chromosome gene repertoire in mammalian species other than human has not been explored until very recently. Here the authors used a directed approach to isolate Y chromosome genes of the domestic cat, an evolutionary divergent species from human and mouse. They found that the feline Y chromosome harbors its own unique set of genes that are expressed specifically in the testes, presumably where they play an important role in spermatogenesis. Paralleling the discoveries seen from the full human Y chromosome sequence, the feline Y chromosome has acquired and remodeled some genes from autosomes, while other genes have a shared ancestry with the X chromosome. However, none of the four new genes are found on the Y chromosomes of human or mouse, although two are shared with the canine Y chromosome. This work highlights the Y chromosome as a source of potential gene novelty in different species and suggests that more directed efforts at characterizing this hitherto understudied chromosome will further enrich our understanding of the types of genes found there and the roles they may play in mammalian spermatogenesis.