The Birth and Death of Olfactory Receptor Gene Families in Mammalian Niche Adaptation

Abstract

The olfactory receptor (OR) gene families, which govern mammalian olfaction, have undergone extensive expansion and contraction through duplication and pseudogenization. Previous studies have shown that broadly defined environmental adaptations (e.g., terrestrial vs. aquatic) are correlated with the number of functional and non-functional OR genes retained. However, to date, no study has examined species-specific gene duplications in multiple phylogenetically divergent mammals to elucidate OR evolution and adaptation. Here, we identify the OR gene families driving adaptation to different ecological niches by mapping the fate of species-specific gene duplications in the OR repertoire of 94 diverse mammalian taxa, using molecular phylogenomic methods. We analyze >70,000 OR gene sequences mined from whole genomes, generated from novel amplicon sequencing data, and collated with data from previous studies, comprising one of the largest OR studies to date. For the first time, we demonstrate statistically significant patterns of OR species-specific gene duplications associated with the presence of a functioning vomeronasal organ. With respect to dietary niche, we uncover a novel link between a large number of duplications in OR family 5/8/9 and herbivory. Our results also highlight differences between social and solitary niches, indicating that a greater OR repertoire expansion may be associated with a solitary lifestyle. This study demonstrates the utility of species-specific duplications in elucidating gene family evolution, revealing how the OR repertoire has undergone expansion and contraction with respect to a number of ecological adaptations in mammals.

Species tree disequilibrium positively misleads models of gene family evolution

“…Based on its expansion within frugivorous phyllostomids, elements of OR subfamily 5/8/9 may therefore specifically respond to volatile organic compounds (VOCs) released by ripening fruits. Indeed, expansions of this subfamily have recently been linked to herbivory in mammals (Hughes et al 2018), lending confidence to the conclusion that OR subfamily 5/8/9 is involved in detecting plant VOCs. It has been previously hypothesized that the size of an OR repertoire could influence olfactory sensitivity {\rtf (Rouquier et al 2000; but see Wackermannová et al, 2016), and some evidence suggests this may be the case (Laska and Shepherd 2007;Rizvanovic et al 2013).…”

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species

“…Indeed, spectacular evidence of molecular convergence has been uncovered in hearing genes in echolocating whales and certain echolocating bats (62)(63)(64)(65). Olfactory receptor genes that are directly involved in olfaction show evidence of environmental niche specialization in aquatic, terrestrial, and flying mammals, even after controlling for phylogeny (31,66,67). Similar loss of function in short-wave opsin visual genes has been found in bats with advanced echolocation capabilities (30).…”

Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

“…Both insect Ors and the phylogenetically unrelated vertebrate Ors are assumed to evolve rapidly following a birth-and-death evolutionary process with new genes being born by gene duplication and others being lost by pseudogenisation (Andersson et al, 2015;Benton, 2015;Hansson and Stensmyr, 2011;Hughes et al, 2018;Nei et al, 2008;Nei and Rooney, 2005;Ramdya and Benton, 2010;Sánchez-Gracia et al, 2009). In combination with the adaptation of the Or repertoire to the species' ecological niche, this evolutionary process leads to Or gene phylogenies mostly lacking clear orthologs between species, and with species-specific expansions and reductions, which do not necessarily follow the underlying species phylogeny.…”