Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs
Abstract Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and...
Gespeichert in:
Veröffentlicht in: | Molecular biology and evolution 2023-10, Vol.40 (10) |
---|---|
Hauptverfasser: | , , , , , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | |
---|---|
container_issue | 10 |
container_start_page | |
container_title | Molecular biology and evolution |
container_volume | 40 |
creator | Wan, Yin Chen Navarrete Méndez, María José O'Connell, Lauren A Uricchio, Lawrence H Roland, Alexandre-Benoit Maan, Martine E Ron, Santiago R Betancourth-Cundar, Mileidy Pie, Marcio R Howell, Kimberly A Richards-Zawacki, Corinne L Cummings, Molly E Cannatella, David C Santos, Juan C Tarvin, Rebecca D |
description | Abstract
Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in frogs and some salamanders, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their behavior. Our analyses show that assessments of opsin diversification in across taxa could expand our understanding of the role of sensory system evolution in ecological adaptation. |
doi_str_mv | 10.1093/molbev/msad206 |
format | Article |
fullrecord | <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10548314</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A775003518</galeid><oup_id>10.1093/molbev/msad206</oup_id><sourcerecordid>A775003518</sourcerecordid><originalsourceid>FETCH-LOGICAL-c492t-50bc9a8eb157540e46d19f94c63fedbc9a4705882bcc16552b8993fb097d78b43</originalsourceid><addsrcrecordid>eNqFkdFrFDEQxoMo9qy--igBX-zDtckm2SRPUmpbC4cVrtXHkM3OXiO7yZrsFvzvzXnXolCQDGSY-c1HMh9Cbyk5pkSzkyH2DdyfDNm2FamfoQUVTC6ppPo5WhBZck6YOkCvcv5BCOW8rl-iAyalplzKBdqsoQc3-RhwiW8-z7bH12P2AV9CgIxL8snPKZTyF4hTiqN3Jb9IcZOxDS1exZxx7PB0B3j9fV3tp0t8jT4X0T_oa_Sis32GN_v7EN1enN-cfV6uri-vzk5XS8d1NS0FaZy2ChoqpOAEeN1S3WnuatZBu-1xSYRSVeMcrYWoGqU16xqiZStVw9kh-rjTHedmgNZBmJLtzZj8YNMvE603_3aCvzObeG8oEVwxulX4sFdI8ecMeTKDzw763gaIczaVkpUinCtR0Pc7dGN7MD50ZT_WbXFzKqUghAmqCnX8BFVOC4N3MUDnS_2pAZfKbhN0j8-nxGxdNzvXzd71MvDu708_4g82F-BoB8R5_J_Yb_hCuC4</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2872804485</pqid></control><display><type>article</type><title>Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs</title><source>Oxford Journals Open Access Collection</source><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Wan, Yin Chen ; Navarrete Méndez, María José ; O'Connell, Lauren A ; Uricchio, Lawrence H ; Roland, Alexandre-Benoit ; Maan, Martine E ; Ron, Santiago R ; Betancourth-Cundar, Mileidy ; Pie, Marcio R ; Howell, Kimberly A ; Richards-Zawacki, Corinne L ; Cummings, Molly E ; Cannatella, David C ; Santos, Juan C ; Tarvin, Rebecca D</creator><creatorcontrib>Wan, Yin Chen ; Navarrete Méndez, María José ; O'Connell, Lauren A ; Uricchio, Lawrence H ; Roland, Alexandre-Benoit ; Maan, Martine E ; Ron, Santiago R ; Betancourth-Cundar, Mileidy ; Pie, Marcio R ; Howell, Kimberly A ; Richards-Zawacki, Corinne L ; Cummings, Molly E ; Cannatella, David C ; Santos, Juan C ; Tarvin, Rebecca D</creatorcontrib><description>Abstract
Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in frogs and some salamanders, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their behavior. Our analyses show that assessments of opsin diversification in across taxa could expand our understanding of the role of sensory system evolution in ecological adaptation.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msad206</identifier><identifier>PMID: 37791477</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Amino acids ; Amphibians ; Analysis ; Animals ; Discoveries ; Frogs ; Genes ; Opsins - genetics ; Phylogeny ; Poisons ; Rod Opsins - genetics</subject><ispartof>Molecular biology and evolution, 2023-10, Vol.40 (10)</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.</rights><rights>COPYRIGHT 2023 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c492t-50bc9a8eb157540e46d19f94c63fedbc9a4705882bcc16552b8993fb097d78b43</citedby><cites>FETCH-LOGICAL-c492t-50bc9a8eb157540e46d19f94c63fedbc9a4705882bcc16552b8993fb097d78b43</cites><orcidid>0000-0001-7611-1215 ; 0000-0003-2368-6028 ; 0000-0001-6300-9350 ; 0000-0001-9514-8945 ; 0000-0002-4212-041X ; 0000-0002-9463-9838 ; 0000-0003-1455-6352 ; 0000-0002-2706-4077 ; 0000-0003-1113-8067 ; 0000-0001-5387-7250</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548314/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548314/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37791477$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wan, Yin Chen</creatorcontrib><creatorcontrib>Navarrete Méndez, María José</creatorcontrib><creatorcontrib>O'Connell, Lauren A</creatorcontrib><creatorcontrib>Uricchio, Lawrence H</creatorcontrib><creatorcontrib>Roland, Alexandre-Benoit</creatorcontrib><creatorcontrib>Maan, Martine E</creatorcontrib><creatorcontrib>Ron, Santiago R</creatorcontrib><creatorcontrib>Betancourth-Cundar, Mileidy</creatorcontrib><creatorcontrib>Pie, Marcio R</creatorcontrib><creatorcontrib>Howell, Kimberly A</creatorcontrib><creatorcontrib>Richards-Zawacki, Corinne L</creatorcontrib><creatorcontrib>Cummings, Molly E</creatorcontrib><creatorcontrib>Cannatella, David C</creatorcontrib><creatorcontrib>Santos, Juan C</creatorcontrib><creatorcontrib>Tarvin, Rebecca D</creatorcontrib><title>Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract
Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in frogs and some salamanders, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their behavior. Our analyses show that assessments of opsin diversification in across taxa could expand our understanding of the role of sensory system evolution in ecological adaptation.</description><subject>Amino acids</subject><subject>Amphibians</subject><subject>Analysis</subject><subject>Animals</subject><subject>Discoveries</subject><subject>Frogs</subject><subject>Genes</subject><subject>Opsins - genetics</subject><subject>Phylogeny</subject><subject>Poisons</subject><subject>Rod Opsins - genetics</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFkdFrFDEQxoMo9qy--igBX-zDtckm2SRPUmpbC4cVrtXHkM3OXiO7yZrsFvzvzXnXolCQDGSY-c1HMh9Cbyk5pkSzkyH2DdyfDNm2FamfoQUVTC6ppPo5WhBZck6YOkCvcv5BCOW8rl-iAyalplzKBdqsoQc3-RhwiW8-z7bH12P2AV9CgIxL8snPKZTyF4hTiqN3Jb9IcZOxDS1exZxx7PB0B3j9fV3tp0t8jT4X0T_oa_Sis32GN_v7EN1enN-cfV6uri-vzk5XS8d1NS0FaZy2ChoqpOAEeN1S3WnuatZBu-1xSYRSVeMcrYWoGqU16xqiZStVw9kh-rjTHedmgNZBmJLtzZj8YNMvE603_3aCvzObeG8oEVwxulX4sFdI8ecMeTKDzw763gaIczaVkpUinCtR0Pc7dGN7MD50ZT_WbXFzKqUghAmqCnX8BFVOC4N3MUDnS_2pAZfKbhN0j8-nxGxdNzvXzd71MvDu708_4g82F-BoB8R5_J_Yb_hCuC4</recordid><startdate>20231004</startdate><enddate>20231004</enddate><creator>Wan, Yin Chen</creator><creator>Navarrete Méndez, María José</creator><creator>O'Connell, Lauren A</creator><creator>Uricchio, Lawrence H</creator><creator>Roland, Alexandre-Benoit</creator><creator>Maan, Martine E</creator><creator>Ron, Santiago R</creator><creator>Betancourth-Cundar, Mileidy</creator><creator>Pie, Marcio R</creator><creator>Howell, Kimberly A</creator><creator>Richards-Zawacki, Corinne L</creator><creator>Cummings, Molly E</creator><creator>Cannatella, David C</creator><creator>Santos, Juan C</creator><creator>Tarvin, Rebecca D</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7611-1215</orcidid><orcidid>https://orcid.org/0000-0003-2368-6028</orcidid><orcidid>https://orcid.org/0000-0001-6300-9350</orcidid><orcidid>https://orcid.org/0000-0001-9514-8945</orcidid><orcidid>https://orcid.org/0000-0002-4212-041X</orcidid><orcidid>https://orcid.org/0000-0002-9463-9838</orcidid><orcidid>https://orcid.org/0000-0003-1455-6352</orcidid><orcidid>https://orcid.org/0000-0002-2706-4077</orcidid><orcidid>https://orcid.org/0000-0003-1113-8067</orcidid><orcidid>https://orcid.org/0000-0001-5387-7250</orcidid></search><sort><creationdate>20231004</creationdate><title>Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs</title><author>Wan, Yin Chen ; Navarrete Méndez, María José ; O'Connell, Lauren A ; Uricchio, Lawrence H ; Roland, Alexandre-Benoit ; Maan, Martine E ; Ron, Santiago R ; Betancourth-Cundar, Mileidy ; Pie, Marcio R ; Howell, Kimberly A ; Richards-Zawacki, Corinne L ; Cummings, Molly E ; Cannatella, David C ; Santos, Juan C ; Tarvin, Rebecca D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c492t-50bc9a8eb157540e46d19f94c63fedbc9a4705882bcc16552b8993fb097d78b43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Amino acids</topic><topic>Amphibians</topic><topic>Analysis</topic><topic>Animals</topic><topic>Discoveries</topic><topic>Frogs</topic><topic>Genes</topic><topic>Opsins - genetics</topic><topic>Phylogeny</topic><topic>Poisons</topic><topic>Rod Opsins - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wan, Yin Chen</creatorcontrib><creatorcontrib>Navarrete Méndez, María José</creatorcontrib><creatorcontrib>O'Connell, Lauren A</creatorcontrib><creatorcontrib>Uricchio, Lawrence H</creatorcontrib><creatorcontrib>Roland, Alexandre-Benoit</creatorcontrib><creatorcontrib>Maan, Martine E</creatorcontrib><creatorcontrib>Ron, Santiago R</creatorcontrib><creatorcontrib>Betancourth-Cundar, Mileidy</creatorcontrib><creatorcontrib>Pie, Marcio R</creatorcontrib><creatorcontrib>Howell, Kimberly A</creatorcontrib><creatorcontrib>Richards-Zawacki, Corinne L</creatorcontrib><creatorcontrib>Cummings, Molly E</creatorcontrib><creatorcontrib>Cannatella, David C</creatorcontrib><creatorcontrib>Santos, Juan C</creatorcontrib><creatorcontrib>Tarvin, Rebecca D</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wan, Yin Chen</au><au>Navarrete Méndez, María José</au><au>O'Connell, Lauren A</au><au>Uricchio, Lawrence H</au><au>Roland, Alexandre-Benoit</au><au>Maan, Martine E</au><au>Ron, Santiago R</au><au>Betancourth-Cundar, Mileidy</au><au>Pie, Marcio R</au><au>Howell, Kimberly A</au><au>Richards-Zawacki, Corinne L</au><au>Cummings, Molly E</au><au>Cannatella, David C</au><au>Santos, Juan C</au><au>Tarvin, Rebecca D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2023-10-04</date><risdate>2023</risdate><volume>40</volume><issue>10</issue><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in frogs and some salamanders, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their behavior. Our analyses show that assessments of opsin diversification in across taxa could expand our understanding of the role of sensory system evolution in ecological adaptation.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>37791477</pmid><doi>10.1093/molbev/msad206</doi><orcidid>https://orcid.org/0000-0001-7611-1215</orcidid><orcidid>https://orcid.org/0000-0003-2368-6028</orcidid><orcidid>https://orcid.org/0000-0001-6300-9350</orcidid><orcidid>https://orcid.org/0000-0001-9514-8945</orcidid><orcidid>https://orcid.org/0000-0002-4212-041X</orcidid><orcidid>https://orcid.org/0000-0002-9463-9838</orcidid><orcidid>https://orcid.org/0000-0003-1455-6352</orcidid><orcidid>https://orcid.org/0000-0002-2706-4077</orcidid><orcidid>https://orcid.org/0000-0003-1113-8067</orcidid><orcidid>https://orcid.org/0000-0001-5387-7250</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0737-4038 |
ispartof | Molecular biology and evolution, 2023-10, Vol.40 (10) |
issn | 0737-4038 1537-1719 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10548314 |
source | Oxford Journals Open Access Collection; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
subjects | Amino acids Amphibians Analysis Animals Discoveries Frogs Genes Opsins - genetics Phylogeny Poisons Rod Opsins - genetics |
title | Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T03%3A35%3A16IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Selection%20on%20Visual%20Opsin%20Genes%20in%20Diurnal%20Neotropical%20Frogs%20and%20Loss%20of%20the%20SWS2%20Opsin%20in%20Poison%20Frogs&rft.jtitle=Molecular%20biology%20and%20evolution&rft.au=Wan,%20Yin%20Chen&rft.date=2023-10-04&rft.volume=40&rft.issue=10&rft.issn=0737-4038&rft.eissn=1537-1719&rft_id=info:doi/10.1093/molbev/msad206&rft_dat=%3Cgale_pubme%3EA775003518%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2872804485&rft_id=info:pmid/37791477&rft_galeid=A775003518&rft_oup_id=10.1093/molbev/msad206&rfr_iscdi=true |