Inactivation of ancV1R as a Predictive Signature for the Loss of Vomeronasal System in Mammals.

Zicong Zhang,Masato Nikaido

doi:10.1093/gbe/evaa082

Abstract

The vomeronasal organ (VNO) plays a key role in sensing pheromonal cues, which elicits social and reproductive behaviors. Although the VNO is highly conserved across mammals, it has been lost in some species that have evolved alternate sensing systems during diversification. In this study, we investigate a newly identified VNO-specific gene, ancV1R, in the extant 261 species of mammals to examine the correlation between genotype (ancV1R) and phenotype (VNO). As a result, we found signatures for the relaxation of purifying selection (inactivating mutations and the elevation of dN/dS) on ancV1Rs in VNO-lacking mammals, such as catarrhine primates, cetaceans, the manatees, and several bat lineages, showing the distinct correlation between genotype and phenotype. Interestingly, we further revealed signatures for the relaxation of purifying selection on ancV1R in true seals, otters, the fossa, the owl monkey, and alcelaphine antelopes in which the existence of a functional VNO is still under debate. Our additional analyses on TRPC2, another predictive marker gene for the functional VNO, showed a relaxation of purifying selection, supporting the possibility of VNO loss in these species. The results of our present study invite more in-depth neuroanatomical investigation in mammals for which VNO function remains equivocal.

Highlights

The vomeronasal organ (VNO) is a chemosensory structure found in terrestrial vertebrates that is anatomically separated from the main olfactory epithelium (MOE)
By applying ancV1R as a reliable diagnostic indicator of VNO function, we revealed the relaxation of purifying selection in ancV1Rs for true seals, the sea otter, the giant otter, the fossa, the owl monkey, and alcelaphine antelopes, in which the existence of a functional VNO is still under debate
We extensively analyzed a total of 298 ancV1R sequences of vertebrates. ancV1Rs were not found in teleosts and birds and were inactivated by many insertions and deletions in crocodilians and testudines, which confirm our previous study (Suzuki et al 2018) and are consistent with the absence of intact VNO in these species (e.g., Silva and Antunes 2017)

Summary

Introduction

The vomeronasal organ (VNO) is a chemosensory structure found in terrestrial vertebrates that is anatomically separated from the main olfactory epithelium (MOE). The VNO structure can be found across a broad diversity of mammals because of its importance to pheromone-mediated communication, essential for fitness and survival (Døving and Trotier 1998). Morphological studies have shown that some mammals do not possess anatomically intact VNOs. For example, cetaceans and sirenians lost the VNO in parallel accompanied by their independent adaptation to fully aquatic lifestyles (Lowell and Flanigan 1980; Switzer et al 1980; Mackay-Sim et al 1985; Oelschl€aiger 1989). Most species have lost their VNO except for two families (Phyllostomidae and Miniopteridae; Wible and Bhatnagar 1996). These independent losses on each bat lineage are still puzzling. Otariids (fur seals, sea lions) and odobenids (walrus) retain the VNO, whereas this organ is lost in phocids (true seals; Mackay-Sim et al 1985)

Methods

Results

Conclusion