Convergent degeneration of olfactory receptor gene repertoires in marine mammals

Ake Liu,Ruixiang Liu,Jingqi Zhou,Zhijun Wang,Libing Shen,Funan He

doi:10.1186/s12864-019-6290-0

Abstract

BackgroundOlfactory receptors (ORs) can bind odor molecules and play a crucial role in odor sensation. Due to the frequent gains and losses of genes during evolution, the number of OR members varies greatly among different species. However, whether the extent of gene gains/losses varies between marine mammals and related terrestrial mammals has not been clarified, and the factors that might underlie these variations are unknown.ResultsTo address these questions, we identified more than 10,000 members of the OR family in 23 mammals and classified them into 830 orthologous gene groups (OGGs) and 281 singletons. Significant differences occurred in the number of OR repertoires and OGGs among different species. We found that all marine mammals had fewer OR genes than their related terrestrial lineages, with the fewest OR genes found in cetaceans, which may be closely related to olfactory degradation. ORs with more gene duplications or loss events tended to be under weaker purifying selection. The average gain and loss rates of OR genes in terrestrial mammals were higher than those of mammalian gene families, while the average gain and loss rates of OR genes in marine mammals were significantly lower and much higher than those of mammalian gene families, respectively. Additionally, we failed to detect any one-to-one orthologous genes in the focal species, suggesting that OR genes are not well conserved among marine mammals.ConclusionsMarine mammals have experienced large numbers of OR gene losses compared with their related terrestrial lineages, which may result from the frequent birth-and-death evolution under varied functional constrains. Due to their independent degeneration, OR genes present in each lineage are not well conserved among marine mammals. Our study provides a basis for future research on the olfactory receptor function in mammals from the perspective of evolutionary trajectories.

Highlights

Olfactory receptors (ORs) can bind odor molecules and play a crucial role in odor sensation
OR gene numbers of marine mammals are significantly lower than those of terrestrial mammals We identified a total of 12,711 intact OR genes from the full genome data of eutherian mammals and the outgroup opossum genome based on protein sequence similarity and homologous relationships
We found that the OR gene numbers in marine mammals were significantly lower than those in closely related terrestrial mammals (Fig. 1b, MannWhitney U test, p value = 2.84 × 10− 6), which is consistent with previous reports

Summary

Introduction

Olfactory receptors (ORs) can bind odor molecules and play a crucial role in odor sensation. Due to the frequent gains and losses of genes during evolution, the number of OR members varies greatly among different species. Olfactory receptors (ORs) can bind odor molecules and are crucial in olfactory sensation [1, 2]. Different amino acid sites play different roles in determining the specificity of receptors. Any OR gene can produce a receptor protein, which helps animals to distinguish many different compounds [5, 6]. According to differences in their amino acid sequences, receptor proteins are usually classified into Class I and Class II proteins [7,8,9]. The majority of ORs in fish are Class I receptors [10], whereas the majority of amphibians and mammals harbor Class II receptors [8]

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