Birth-and-death evolution of ribonuclease 9 genes in Cetartiodactyla

RNase9 plays a reproductive function and has been recognized as an important member of the ribonuclease (RNase) A superfamily, a gene family that is widely used as a model for molecular evolutionary studies. Here, we identified 178 RNase9 genes from 95 Cetartiodactyla species that represent all four lineages and 21 families of this clade. Unexpectedly, RNase9 experienced an evolutionary scenario of "birth and death" in Ruminantia, and expression analyses showed that duplicated RNase9A and RNase9B genes are expressed in reproductive tissues (epididymis, vas deferens or prostate). This expression pattern combined with the estimate that these genes duplicated during the middle Eocene, a time when Ruminantia become a successful lineage, suggests that the RNase9 gene duplication might have been advantageous for promoting sperm motility and male fertility as an adaptation to climate seasonality changes of this period. In contrast, all RNase9 genes were lost in the Cetacean lineage, which might be associated with their high levels of prostatic lesions and lower reproductive rates as adaptations to a fully aquatic environment and a balance to the demands of ocean resources. This study reveals a complex and intriguing evolutionary history and functional divergence for RNase9 in Cetartiodactyla, providing new insights into the evolution of the RNaseA superfamily and molecular mechanisms for organismal adaptations to the environment.