Lineage-specific duplication and adaptive evolution of bitter taste receptor genes in bats

By generating raw genetic material and diverse biological functions, gene duplication represents a major evolutionary mechanism that is of fundamental importance in ecological adaptation. The lineage-specific duplication events of bitter taste receptor genes (Tas2rs) have been identified in a number of vertebrates, but functional evolution of new Tas2r copies after duplication remains largely unknown. Here, we present the largest data set of bat Tas2rs to date, identified from existing genome sequences of 15 bat species and newly sequenced from 17 bat species, and demonstrate lineage-specific duplications of Tas2r16, Tas2r18 and Tas2r41 that only occurred in Myotis bats. Myotis bats are highly speciose and represent the only mammalian genus that is naturally distributed on every continent except Antarctica. The occupation of such diverse habitats might have driven the Tas2r gene expansion. New copies of Tas2rs in Myotis bats have shown molecular adaptation and functional divergence. For example, three copies of Tas2r16 in Myotis davidii showed differential sensitivities to arbutin and salicin that may occur in their insect prey, as suggested by cell-based functional assays. We hypothesize that functional differences among Tas2r copies in Myotis bats would increase their survival rate through preventing the ingestion of an elevated number of bitter-tasting dietary toxins from their insect prey, which may have facilitated their adaptation to diverse habitats. Our study demonstrates functional changes of new Tas2r copies after lineage-specific duplications in Myotis bats and highlights the potential role of taste perception in exploiting new environments.