Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication, surviving opsins and spectral tuning
Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution...
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Veröffentlicht in: | Molecular ecology 2020-06, Vol.29 (12), p.2234-2253 |
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description | Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2‐chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS‐ and RH1‐duplicates originated from a teleost specific whole‐genome duplication as well as characiform‐specific duplication events. Both LWS‐opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS‐paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS‐paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A1/A2‐chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved. |
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R.</creator><creatorcontrib>Escobar‐Camacho, Daniel ; Carleton, Karen L. ; Narain, Devika W. ; Pierotti, Michele E. R.</creatorcontrib><description>Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2‐chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS‐ and RH1‐duplicates originated from a teleost specific whole‐genome duplication as well as characiform‐specific duplication events. Both LWS‐opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS‐paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS‐paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A1/A2‐chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.15474</identifier><identifier>PMID: 32421918</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Adaptation ; Amino acid sequence ; Amino acids ; Characiformes ; chromophore ; Chromophores ; Color vision ; Conversion ; Evolution ; Gene conversion ; Gene duplication ; genome duplication ; Genomes ; Genotypes ; Information processing ; Interspecific ; opsin ; Opsins ; Phenotypes ; Photopigments ; Reproduction (copying) ; Reversion ; Spectra ; Spectral sensitivity ; spectral tuning ; Tuning ; Visual aspects ; visual pigment ; Visual pigments ; Visual system</subject><ispartof>Molecular ecology, 2020-06, Vol.29 (12), p.2234-2253</ispartof><rights>2020 John Wiley & Sons Ltd</rights><rights>This article is protected by copyright. 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R.</creatorcontrib><title>Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication, surviving opsins and spectral tuning</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2‐chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS‐ and RH1‐duplicates originated from a teleost specific whole‐genome duplication as well as characiform‐specific duplication events. Both LWS‐opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS‐paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS‐paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A1/A2‐chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved.</description><subject>Adaptation</subject><subject>Amino acid sequence</subject><subject>Amino acids</subject><subject>Characiformes</subject><subject>chromophore</subject><subject>Chromophores</subject><subject>Color vision</subject><subject>Conversion</subject><subject>Evolution</subject><subject>Gene conversion</subject><subject>Gene duplication</subject><subject>genome duplication</subject><subject>Genomes</subject><subject>Genotypes</subject><subject>Information processing</subject><subject>Interspecific</subject><subject>opsin</subject><subject>Opsins</subject><subject>Phenotypes</subject><subject>Photopigments</subject><subject>Reproduction (copying)</subject><subject>Reversion</subject><subject>Spectra</subject><subject>Spectral sensitivity</subject><subject>spectral tuning</subject><subject>Tuning</subject><subject>Visual aspects</subject><subject>visual pigment</subject><subject>Visual pigments</subject><subject>Visual system</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp1kcuKFDEUhoMoTs_owheQgBsHrJlcTt1cCNKMFxhxM4q7kE6d6s6QSmqSqh565wO48Bl9EjP2OKhgNiH8H1_O4SfkCWcnPJ_TAc0JL6GGe2TBZVUWooUv98mCtZUoOGvkATlM6ZIxLkVZPiQHUoDgLW8W5Ntnm2bt6GjXA_qJ4ja4ebLBU-vpcqOjNrYPccD0kl5skHY7rwdrcjphHJ3e0dDTCR2GNNHrTXD44-v3NfowZHYenTX6xvaCpjlu7db6NQ1jsj5R7TuaRjRTzN9Ps8_RI_Kg1y7h49v7iHx6c3axfFecf3z7fvn6vDAAEop6VWPVyV5IbbSBtqlNJ3owgucHlBKxERJ0bfqVKbsVZxWg6QChM0bLCuURebX3jvNqwM7kxfMQaox20HGngrbq78TbjVqHraqh5MDqLHh-K4jhasY0qcEmg85pj2FOSgCDSrY1sIw--we9DHP0eb1M8baRTV3JTB3vKRNDShH7u2E4Uzcdq9yx-tVxZp_-Of0d-bvUDJzugWvrcPd_k_pwttwrfwIq_bax</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Escobar‐Camacho, Daniel</creator><creator>Carleton, Karen L.</creator><creator>Narain, Devika W.</creator><creator>Pierotti, Michele E. R.</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2837-6192</orcidid><orcidid>https://orcid.org/0000-0001-6660-4331</orcidid><orcidid>https://orcid.org/0000-0001-6306-5643</orcidid></search><sort><creationdate>202006</creationdate><title>Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication, surviving opsins and spectral tuning</title><author>Escobar‐Camacho, Daniel ; Carleton, Karen L. ; Narain, Devika W. ; Pierotti, Michele E. 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R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication, surviving opsins and spectral tuning</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2020-06</date><risdate>2020</risdate><volume>29</volume><issue>12</issue><spage>2234</spage><epage>2253</epage><pages>2234-2253</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2‐chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS‐ and RH1‐duplicates originated from a teleost specific whole‐genome duplication as well as characiform‐specific duplication events. Both LWS‐opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS‐paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS‐paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A1/A2‐chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32421918</pmid><doi>10.1111/mec.15474</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0003-2837-6192</orcidid><orcidid>https://orcid.org/0000-0001-6660-4331</orcidid><orcidid>https://orcid.org/0000-0001-6306-5643</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation Amino acid sequence Amino acids Characiformes chromophore Chromophores Color vision Conversion Evolution Gene conversion Gene duplication genome duplication Genomes Genotypes Information processing Interspecific opsin Opsins Phenotypes Photopigments Reproduction (copying) Reversion Spectra Spectral sensitivity spectral tuning Tuning Visual aspects visual pigment Visual pigments Visual system |
title | Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication, surviving opsins and spectral tuning |
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