Convergent degeneration of olfactory receptor gene repertoires in marine mammals

Abstract Background 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. However, whether the extent of gene gains/losses varies be...

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Main Authors: Ake Liu, Funan He, Libing Shen, Ruixiang Liu, Zhijun Wang, Jingqi Zhou
Format: Article
Language:English
Published: BMC 2019-12-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-019-6290-0
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spelling doaj-227858ef10464b4587f2aaf667d09eef2020-12-13T12:18:11ZengBMCBMC Genomics1471-21642019-12-0120111410.1186/s12864-019-6290-0Convergent degeneration of olfactory receptor gene repertoires in marine mammalsAke Liu0Funan He1Libing Shen2Ruixiang Liu3Zhijun Wang4Jingqi Zhou5Faculty of Biological Science and Technology, Changzhi UniversitySchool of Life Sciences, Fudan UniversityInstitute of Neuroscience, Shanghai Institute for Biological Sciences, Chinese Academy of SciencesFaculty of Biological Science and Technology, Changzhi UniversityDepartment of Chemistry, Changzhi UniversitySchool of Public Health, Shanghai Jiao Tong University School of MedicineAbstract Background 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. 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. Results To 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. Conclusions Marine 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.https://doi.org/10.1186/s12864-019-6290-0Olfactory receptorsMarine mammalsConvergent degenerationGene gainGene lossOrthologous gene groups
collection DOAJ
language English
format Article
sources DOAJ
author Ake Liu
Funan He
Libing Shen
Ruixiang Liu
Zhijun Wang
Jingqi Zhou
spellingShingle Ake Liu
Funan He
Libing Shen
Ruixiang Liu
Zhijun Wang
Jingqi Zhou
Convergent degeneration of olfactory receptor gene repertoires in marine mammals
BMC Genomics
Olfactory receptors
Marine mammals
Convergent degeneration
Gene gain
Gene loss
Orthologous gene groups
author_facet Ake Liu
Funan He
Libing Shen
Ruixiang Liu
Zhijun Wang
Jingqi Zhou
author_sort Ake Liu
title Convergent degeneration of olfactory receptor gene repertoires in marine mammals
title_short Convergent degeneration of olfactory receptor gene repertoires in marine mammals
title_full Convergent degeneration of olfactory receptor gene repertoires in marine mammals
title_fullStr Convergent degeneration of olfactory receptor gene repertoires in marine mammals
title_full_unstemmed Convergent degeneration of olfactory receptor gene repertoires in marine mammals
title_sort convergent degeneration of olfactory receptor gene repertoires in marine mammals
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-12-01
description Abstract Background 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. 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. Results To 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. Conclusions Marine 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.
topic Olfactory receptors
Marine mammals
Convergent degeneration
Gene gain
Gene loss
Orthologous gene groups
url https://doi.org/10.1186/s12864-019-6290-0
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AT ruixiangliu convergentdegenerationofolfactoryreceptorgenerepertoiresinmarinemammals
AT zhijunwang convergentdegenerationofolfactoryreceptorgenerepertoiresinmarinemammals
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