Massive Loss of Olfactory Receptors But Not Trace Amine-Associated Receptors in the World's Deepest-Living Fish (Pseudoliparis swirei).

Haifeng Jiang,Liandong Yang,Xiaoni Gan,Kang Du,Shunping He

doi:10.3390/genes10110910

Abstract

Olfactory receptor repertoires show highly dynamic evolution associated with ecological adaptations in different species. The Mariana snailfish (Pseudoliparis swirei) living below a depth of 6000 m in the Mariana Trench evolved degraded vision and occupies a specific feeding habitat in a dark, low-food environment. However, whether such adaptations involve adaptive changes in the chemosensory receptor repertoire is not known. Here, we conducted a comparative analysis of the olfactory receptor (OR) and trace amine-associated receptor (TAAR) gene repertoires in nine teleosts with a focus on the evolutionary divergence between the Mariana snailfish and its shallow-sea relative, Tanaka’s snailfish (Liparis tanakae). We found many fewer functional OR genes and a significantly higher fraction of pseudogenes in the Mariana snailfish, but the numbers of functional TAAR genes in the two species were comparable. Phylogenetic analysis showed that the expansion patterns of the gene families were shared by the two species, but that Mariana snailfish underwent massive gene losses in its OR repertoire. Despite an overall decreased size in OR subfamilies and a reduced number of TAAR subfamilies in the Mariana snailfish, expansion of certain subfamilies was observed. Selective pressure analysis indicated greatly relaxed selective strength in ORs but a slightly enhanced selective strength in TAARs of Mariana snailfish. Overall, our study reveals simplified but specific OR and TAAR repertoires in the Mariana snailfish shaped by natural selection with respect to ecological adaptations in the hadal environment. This is the first study on the chemosensation evolution in vertebrates living in the hadal zone, which could provide new insights into evolutionary adaptation to the hadal environment.

Highlights

Olfaction is a typical chemosensation that forms the sense of smell and is essential for the survival and reproduction of various organisms
It is likely that the number of olfactory receptor (OR) subfamilies correlates with odorant discrimination ability because ORs that share less sequence homology are expected to bind different sets of odorants, while the number of ORs in certain subfamilies is correlated with sensitivity to particular odorants due to the presence of similar binding sites that interact with similar molecular structures [12,51,52]. Consistent with this possibility, we found that distinct subfamilies of both the OR and trace amine-associated receptor (TAAR) gene families evolved independently; this can be considered a response to different chemical cues that are relevant in each species’ particular ecological niche
This study reveals the first comparative analysis of the chemosensation evolution in the Mariana snailfish, the world deepest-living vertebrate

Summary

Introduction

Olfaction is a typical chemosensation that forms the sense of smell and is essential for the survival and reproduction of various organisms. The OR genes, which belong to the superfamily of rhodopsin-like G-protein-coupled receptors (GPCRs), form the largest multigene family in mammals. The OR gene family contains 800–1200 functional OR genes in mice, dogs, cows, and horses and more than 2000 genes in African elephants [2]. Each functional OR gene encodes a unique receptor protein that is tuned to a specific set of odorant molecules, and one odorant is generally recognized by diverse combinations of OR genes [4]. This combinatorial receptor coding scheme enables the olfactory system to recognize and discriminate a vast diversity of odorant information that exceeds the limited numbers of receptors

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