Adaptive evolution of pancreatic ribonuclease gene (RNase1) in Cetartiodactyla

Abstract

Pancreatic ribonuclease (RNase1), a digestive enzyme produced by the pancreas, is associated with the functional adaptation of dietary habits and is regarded as an attractive model system for studies of molecular evolution. In this study, we identified 218 functional genes and 48 pseudogenes from 114 species that span all four Cetartiodactyla lineages: two herbivorous lineages (Ruminantia and Tylopoda) and two non‐herbivorous lineages (Cetancodonta and Suoidea). Multiple RNase1 genes were detected in all species of the two herbivorous lineages, and phylogenetic and genomic location analyses demonstrated that independent gene duplication events occurred in Ruminantia and Tylopoda. In Ruminantia, the gene duplication events occurred in the ancestral branches of the lineage in the Middle Eocene, a time of increasing climatic seasonality during which Ruminantia rapidly radiated. In contrast, only a single RNase1 gene was observed in the species of the two non‐herbivorous lineages (Cetancodonta and Suoidea), suggesting that the previous Cetacea‐specific loss hypothesis should be rejected. Moreover, the duplicated genes of RNase1 in the two herbivorous lineages (Ruminantia and Tylopoda) may have undergone functional divergence. In combination with the temporal coincidence between gene replication and the enhanced climatic seasonality during the Middle Eocene, this functional divergence suggests that RNase1 gene duplication was beneficial for Ruminantia to use the limited quantities of sparse fibrous vegetation and adapt to seasonal changes in climate. In summary, the findings indicate a complex and intriguing evolutionary pattern of RNase1 in Cetartiodactyla and demonstrate the molecular mechanisms by which organisms adapt to the environment.