Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes
Abstract Background Ray-finned fishes (Actinopterygii) perceive their environment through a range of sensory modalities, including olfaction. Anatomical diversity of the olfactory organ suggests that olfaction is differentially important among species. To explore this topic, we studied the evolution...
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01397-x |
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| author | Maxime Policarpo Katherine E. Bemis Patrick Laurenti Laurent Legendre Jean-Christophe Sandoz Sylvie Rétaux Didier Casane |
| author_facet | Maxime Policarpo Katherine E. Bemis Patrick Laurenti Laurent Legendre Jean-Christophe Sandoz Sylvie Rétaux Didier Casane |
| author_sort | Maxime Policarpo |
| collection | DOAJ |
| description | Abstract Background Ray-finned fishes (Actinopterygii) perceive their environment through a range of sensory modalities, including olfaction. Anatomical diversity of the olfactory organ suggests that olfaction is differentially important among species. To explore this topic, we studied the evolutionary dynamics of the four main gene families (OR, TAAR, ORA/VR1 and OlfC/VR2) coding for olfactory receptors in 185 species of ray-finned fishes. Results The large variation in the number of functional genes, between 28 in the ocean sunfish Mola mola and 1317 in the reedfish Erpetoichthys calabaricus, is the result of parallel expansions and contractions of the four main gene families. Several ancient and independent simplifications of the olfactory organ are associated with massive gene losses. In contrast, Polypteriformes, which have a unique and complex olfactory organ, have almost twice as many olfactory receptor genes as any other ray-finned fish. Conclusions We document a functional link between morphology of the olfactory organ and richness of the olfactory receptor repertoire. Further, our results demonstrate that the genomic underpinning of olfaction in ray-finned fishes is heterogeneous and presents a dynamic pattern of evolutionary expansions, simplifications, and reacquisitions. |
| first_indexed | 2024-04-14T00:11:21Z |
| format | Article |
| id | doaj.art-506e133d2d964d47a5512e767f230d67 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-14T00:11:21Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-506e133d2d964d47a5512e767f230d672022-12-22T02:23:19ZengBMCBMC Biology1741-70072022-09-0120111010.1186/s12915-022-01397-xCoevolution of the olfactory organ and its receptor repertoire in ray-finned fishesMaxime Policarpo0Katherine E. Bemis1Patrick Laurenti2Laurent Legendre3Jean-Christophe Sandoz4Sylvie Rétaux5Didier Casane6Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et ÉcologieNOAA National Systematics Laboratory, National Museum of Natural History, Smithsonian InstitutionUniversité Paris Cité, Laboratoire Interdisciplinaire des Energies de DemainUniversité Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et ÉcologieUniversité Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et ÉcologieUniversité Paris-Saclay, CNRS, Institut des Neurosciences Paris-SaclayUniversité Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et ÉcologieAbstract Background Ray-finned fishes (Actinopterygii) perceive their environment through a range of sensory modalities, including olfaction. Anatomical diversity of the olfactory organ suggests that olfaction is differentially important among species. To explore this topic, we studied the evolutionary dynamics of the four main gene families (OR, TAAR, ORA/VR1 and OlfC/VR2) coding for olfactory receptors in 185 species of ray-finned fishes. Results The large variation in the number of functional genes, between 28 in the ocean sunfish Mola mola and 1317 in the reedfish Erpetoichthys calabaricus, is the result of parallel expansions and contractions of the four main gene families. Several ancient and independent simplifications of the olfactory organ are associated with massive gene losses. In contrast, Polypteriformes, which have a unique and complex olfactory organ, have almost twice as many olfactory receptor genes as any other ray-finned fish. Conclusions We document a functional link between morphology of the olfactory organ and richness of the olfactory receptor repertoire. Further, our results demonstrate that the genomic underpinning of olfaction in ray-finned fishes is heterogeneous and presents a dynamic pattern of evolutionary expansions, simplifications, and reacquisitions.https://doi.org/10.1186/s12915-022-01397-xOlfactory epitheliumOlfactory lamellaeOlfactory receptor genesActinopterygiiGene family dynamics |
| spellingShingle | Maxime Policarpo Katherine E. Bemis Patrick Laurenti Laurent Legendre Jean-Christophe Sandoz Sylvie Rétaux Didier Casane Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes BMC Biology Olfactory epithelium Olfactory lamellae Olfactory receptor genes Actinopterygii Gene family dynamics |
| title | Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes |
| title_full | Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes |
| title_fullStr | Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes |
| title_full_unstemmed | Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes |
| title_short | Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes |
| title_sort | coevolution of the olfactory organ and its receptor repertoire in ray finned fishes |
| topic | Olfactory epithelium Olfactory lamellae Olfactory receptor genes Actinopterygii Gene family dynamics |
| url | https://doi.org/10.1186/s12915-022-01397-x |
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