Ecological adaptation determines functional mammalian olfactory subgenomes

Abstract

The ability to smell is governed by the largest gene family in mammalian genomes, the olfactory receptor (OR) genes. Although these genes are well annotated in the finished human and mouse genomes, we still do not understand which receptors bind specific odorants or how they fully function. Previous comparative studies have been taxonomically limited and mostly focused on the percentage of OR pseudogenes within species. No study has investigated the adaptive changes of functional OR gene families across phylogenetically and ecologically diverse mammals. To determine the extent to which OR gene repertoires have been influenced by habitat, sensory specialization, and other ecological traits, to better understand the functional importance of specific OR gene families and thus the odorants they bind, we compared the functional OR gene repertoires from 50 mammalian genomes. We amplified more than 2000 OR genes in aquatic, semi-aquatic, and flying mammals and coupled these data with 48,000 OR genes from mostly terrestrial mammals, extracted from genomic projects. Phylogenomic, Bayesian assignment, and principle component analyses partitioned species by ecotype (aquatic, semi-aquatic, terrestrial, flying) rather than phylogenetic relatedness, and identified OR families important for each habitat. Functional OR gene repertoires were reduced independently in the multiple origins of aquatic mammals and were significantly divergent in bats. We reject recent neutralist views of olfactory subgenome evolution and correlate specific OR gene families with physiological requirements, a preliminary step toward unraveling the relationship between specific odors and respective OR gene families.

The influence of nasal airflow on respiratory and olfactory epithelial distribution in felids

“…In general, cats are regarded as macrosmatic animals, though they are thought to have a weaker sense of smell than dogs, based on their behavior and a comparison of the number of functional olfactory receptor genes in both species (Hayden et al, 2010). Cats are carnivorans, and as such, possess a macrosmatic nasal airway architecture consisting of a dorsal meatus and an olfactory recess (Figs 1, 2).…”

Aquatic adaptations in the nose of carnivorans: evidence from the turbinates

“…Nevertheless, all of these studies and ours came to similar conclusions. Moreover, a reduction in olfactory function in aquatic and semi-aquatic species was further implicated by a recent analysis of olfactory receptor (OR) gene repertoires in 50 mammals that revealed a repeated, convergent loss of functional OR gene families in these species relative to terrestrial species (Hayden et al 2010).…”

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).…”

“…Animal genomes are increasingly revealing the genetic basis of environmental niche specialization and adaptation (30)(31)(32)(33), and studying the molecular mechanisms responsible for this diversity has allowed some of the greatest insights into the functioning and evolution of our own genome (32,34,35). Some of the most important challenges facing humanity into the next century are biological.…”