Phylogenomic analyses reveal a molecular signature linked to subterranean adaptation in rodents

Abstract

Background: Genome-wide signatures of convergent evolution are widely expected but rarely revealed in animals. Subterranean rodent genome and transcriptome data produced by next-generation sequencing facilitate the use of phylogenetic methods to infer non-synonymous and synonymous substitution rates within coding regions, which can reveal changes at the molecular level that are correlated with the dramatic shift from a terrestrial to subterranean habitat. Results: Our study used previously sequenced genome or transcriptome data of two subterranean rodents, the blind mole rat and naked mole rat, and their terrestrial relatives, the mouse and Guinea pig, to investigate the genetic basis of rodent subterranean adaptation. An analysis of 4996 orthologous genes revealed that the substitution pace of coding sequences was significantly slower in the blind mole rat than in the mouse, and slower in the naked mole rat than in the Guinea pig. The dN/dS ratio was significantly higher in the blind mole rat than in the mouse and in the naked mole rat than in the Guinea pig. These patterns are most likely related to the longer generation time and lower effective population size of subterranean rodents caused by subterranean ecological constraints. We also identified some genes and gene ontology (GO) categories that might be candidates for adaptation to subterranean life. Conclusions: Our study reveals a case of subterranean convergent evolution in rodents that is correlated with change in the pace and mode of molecular evolution observed at the genome scale. We believe that this genomic signature could have also evolved in other cases of subterranean convergence. Additionally, the genes that displayed the most radical changes in their patterns of evolution and their associated GO categories provide a strong basis for further comparative and functional studies, and potentially reveal molecular signatures of adaptation to subterranean life.