Expanded olfactory system in ray-finned fishes capable of terrestrial exploration
Abstract Background Smell abilities differ greatly among vertebrate species due to distinct sensory needs, with exceptional variability reported in the number of olfactory genes and the size of the odour-processing regions of the brain. However, key environmental factors shaping genomic and phenotyp...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01661-8 |
| _version_ | 1797752633507708928 |
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| author | Demian Burguera Francesco Dionigi Kristina Kverková Sylke Winkler Thomas Brown Martin Pippel Yicheng Zhang Maxwell Shafer Annika L. A. Nichols Eugene Myers Pavel Němec Zuzana Musilova |
| author_facet | Demian Burguera Francesco Dionigi Kristina Kverková Sylke Winkler Thomas Brown Martin Pippel Yicheng Zhang Maxwell Shafer Annika L. A. Nichols Eugene Myers Pavel Němec Zuzana Musilova |
| author_sort | Demian Burguera |
| collection | DOAJ |
| description | Abstract Background Smell abilities differ greatly among vertebrate species due to distinct sensory needs, with exceptional variability reported in the number of olfactory genes and the size of the odour-processing regions of the brain. However, key environmental factors shaping genomic and phenotypic changes linked to the olfactory system remain difficult to identify at macroevolutionary scales. Here, we investigate the association between diverse ecological traits and the number of olfactory chemoreceptors in approximately two hundred ray-finned fishes. Results We found independent expansions producing large gene repertoires in several lineages of nocturnal amphibious fishes, generally able to perform active terrestrial exploration. We reinforced this finding with on-purpose genomic and transcriptomic analysis of Channallabes apus, a catfish species from a clade with chemosensory-based aerial orientation. Furthermore, we also detected an augmented information-processing capacity in the olfactory bulb of nocturnal amphibious fishes by estimating the number of cells contained in this brain region in twenty-four actinopterygian species. Conclusions Overall, we report a convergent genomic and phenotypic magnification of the olfactory system in nocturnal amphibious fishes. This finding suggests the possibility of an analogous evolutionary event in fish-like tetrapod ancestors during the first steps of the water-to-land transition, favouring terrestrial adaptation through enhanced aerial orientation. |
| first_indexed | 2024-03-12T17:06:15Z |
| format | Article |
| id | doaj.art-a02ea485c22e43579ad0100d7b51412a |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-12T17:06:15Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-a02ea485c22e43579ad0100d7b51412a2023-08-06T11:24:51ZengBMCBMC Biology1741-70072023-07-0121111310.1186/s12915-023-01661-8Expanded olfactory system in ray-finned fishes capable of terrestrial explorationDemian Burguera0Francesco Dionigi1Kristina Kverková2Sylke Winkler3Thomas Brown4Martin Pippel5Yicheng Zhang6Maxwell Shafer7Annika L. A. Nichols8Eugene Myers9Pavel Němec10Zuzana Musilova11Department of Zoology, Faculty of Science, Charles UniversityDepartment of Zoology, Faculty of Science, Charles UniversityDepartment of Zoology, Faculty of Science, Charles UniversityMax Planck Institute of Molecular Cell Biology and GeneticsMax Planck Institute of Molecular Cell Biology and GeneticsMax Planck Institute of Molecular Cell Biology and GeneticsDepartment of Zoology, Faculty of Science, Charles UniversityBiozentrum, University of BaselBiozentrum, University of BaselMax Planck Institute of Molecular Cell Biology and GeneticsDepartment of Zoology, Faculty of Science, Charles UniversityDepartment of Zoology, Faculty of Science, Charles UniversityAbstract Background Smell abilities differ greatly among vertebrate species due to distinct sensory needs, with exceptional variability reported in the number of olfactory genes and the size of the odour-processing regions of the brain. However, key environmental factors shaping genomic and phenotypic changes linked to the olfactory system remain difficult to identify at macroevolutionary scales. Here, we investigate the association between diverse ecological traits and the number of olfactory chemoreceptors in approximately two hundred ray-finned fishes. Results We found independent expansions producing large gene repertoires in several lineages of nocturnal amphibious fishes, generally able to perform active terrestrial exploration. We reinforced this finding with on-purpose genomic and transcriptomic analysis of Channallabes apus, a catfish species from a clade with chemosensory-based aerial orientation. Furthermore, we also detected an augmented information-processing capacity in the olfactory bulb of nocturnal amphibious fishes by estimating the number of cells contained in this brain region in twenty-four actinopterygian species. Conclusions Overall, we report a convergent genomic and phenotypic magnification of the olfactory system in nocturnal amphibious fishes. This finding suggests the possibility of an analogous evolutionary event in fish-like tetrapod ancestors during the first steps of the water-to-land transition, favouring terrestrial adaptation through enhanced aerial orientation.https://doi.org/10.1186/s12915-023-01661-8Sensory evolutionAmphibious fishesOlfactory receptorsEvolutionary transition |
| spellingShingle | Demian Burguera Francesco Dionigi Kristina Kverková Sylke Winkler Thomas Brown Martin Pippel Yicheng Zhang Maxwell Shafer Annika L. A. Nichols Eugene Myers Pavel Němec Zuzana Musilova Expanded olfactory system in ray-finned fishes capable of terrestrial exploration BMC Biology Sensory evolution Amphibious fishes Olfactory receptors Evolutionary transition |
| title | Expanded olfactory system in ray-finned fishes capable of terrestrial exploration |
| title_full | Expanded olfactory system in ray-finned fishes capable of terrestrial exploration |
| title_fullStr | Expanded olfactory system in ray-finned fishes capable of terrestrial exploration |
| title_full_unstemmed | Expanded olfactory system in ray-finned fishes capable of terrestrial exploration |
| title_short | Expanded olfactory system in ray-finned fishes capable of terrestrial exploration |
| title_sort | expanded olfactory system in ray finned fishes capable of terrestrial exploration |
| topic | Sensory evolution Amphibious fishes Olfactory receptors Evolutionary transition |
| url | https://doi.org/10.1186/s12915-023-01661-8 |
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