Conservation and selective pressures shaping baleen whale olfactory receptor genes supports their use of olfaction in the marine environment

Abstract

The relative importance of various sensory modalities can shift in response to evolutionary transitions, resulting in changes to underlying gene families encoding their reception systems. The rapid birth-and-death process underlying the evolution of the large olfactory receptor (OR) gene family has accelerated genomic-level change for the sense of smell in particular. The transition from the land to sea in marine mammals is an attractive model for understanding the influence of habitat shifts on sensory systems, with the retained OR repertoire of baleen whales contrasting with its loss in toothed whales. In this study, we examine to what extent the transition from a terrestrial to a marine environment has influenced the evolution of baleen whale OR repertoires. We developed Gene Mining Pipeline (GMPipe) (https://github.com/AprilJauhal/GMPipe), which can accurately identify large numbers of candidate OR genes. GMPipe identified 707 OR sequences from eight baleen whale species. These repertoires exhibited distinct family count distributions compared to terrestrial mammals, including signs of relative expansion in families OR10, OR11 and OR13. While many receptors have been lost or show signs of random drift in baleen whales, others exhibit signs of evolving under purifying or positive selection. Over 85% of OR genes could be sorted into orthologous groups of sequences containing at least four homologous sequences. Many of these groups, particularly from family OR10, presented signs of relative expansion and purifying selective pressure. Overall, our results suggest that the relatively small size of baleen whale OR repertoires result from specialisation to novel olfactory landscapes, as opposed to random drift.