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The Genome of Shaw’s Sea Snake (Hydrophis curtus) Reveals Secondary Adaptation to Its Marine Environment
The transition of terrestrial snakes to marine life ∼10 Ma is ideal for exploring adaptive evolution. Sea snakes possess phenotype specializations including laterally compressed bodies, paddle-shaped tails, valvular nostrils, cutaneous respiration, elongated lungs, and salt glands, yet, knowledge on...
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Published in: | Molecular biology and evolution 2020-06, Vol.37 (6), p.1744-1760 |
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container_title | Molecular biology and evolution |
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creator | Peng, Changjun Ren, Jin-Long Deng, Cao Jiang, Dechun Wang, Jichao Qu, Jiangyong Chang, Jiang Yan, Chaochao Jiang, Ke Murphy, Robert W Wu, Dong-Dong Li, Jia-Tang |
description | The transition of terrestrial snakes to marine life ∼10 Ma is ideal for exploring adaptive evolution. Sea snakes possess phenotype specializations including laterally compressed bodies, paddle-shaped tails, valvular nostrils, cutaneous respiration, elongated lungs, and salt glands, yet, knowledge on the genetic underpinnings of the transition remains limited. Herein, we report the first genome of Shaw’s sea snake (Hydrophis curtus) and use it to investigate sea snake secondary marine adaptation. A hybrid assembly strategy obtains a high-quality genome. Gene family analyses date a pulsed coding-gene expansion to ∼20 Ma, and these genes associate strongly with adaptations to marine environments. Analyses of selection pressure and convergent evolution discover the rapid evolution of protein-coding genes, and some convergent features. Additionally, 108 conserved noncoding elements appear to have evolved quickly, and these may underpin the phenotypic changes. Transposon elements may contribute to adaptive specializations by inserting into genomic regions around functionally related coding genes. The integration of genomic and transcriptomic analyses indicates independent origins and different components in sea snake and terrestrial snake venom; the venom gland of the sea snake harbors the highest PLA2 (17.23%) expression in selected elapids and these genes may organize tandemly in the genome. These analyses provide insights into the genetic mechanisms that underlay the secondary adaptation to marine and venom production of this sea snake. |
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Sea snakes possess phenotype specializations including laterally compressed bodies, paddle-shaped tails, valvular nostrils, cutaneous respiration, elongated lungs, and salt glands, yet, knowledge on the genetic underpinnings of the transition remains limited. Herein, we report the first genome of Shaw’s sea snake (Hydrophis curtus) and use it to investigate sea snake secondary marine adaptation. A hybrid assembly strategy obtains a high-quality genome. Gene family analyses date a pulsed coding-gene expansion to ∼20 Ma, and these genes associate strongly with adaptations to marine environments. Analyses of selection pressure and convergent evolution discover the rapid evolution of protein-coding genes, and some convergent features. Additionally, 108 conserved noncoding elements appear to have evolved quickly, and these may underpin the phenotypic changes. Transposon elements may contribute to adaptive specializations by inserting into genomic regions around functionally related coding genes. The integration of genomic and transcriptomic analyses indicates independent origins and different components in sea snake and terrestrial snake venom; the venom gland of the sea snake harbors the highest PLA2 (17.23%) expression in selected elapids and these genes may organize tandemly in the genome. These analyses provide insights into the genetic mechanisms that underlay the secondary adaptation to marine and venom production of this sea snake.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msaa043</identifier><identifier>PMID: 32077944</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Adaptation, Biological ; Animals ; Aquatic Organisms ; DNA Transposable Elements ; Evolution, Molecular ; Female ; Genome ; Hydrophiidae - genetics ; Molecular Sequence Annotation ; Multigene Family</subject><ispartof>Molecular biology and evolution, 2020-06, Vol.37 (6), p.1744-1760</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. 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Sea snakes possess phenotype specializations including laterally compressed bodies, paddle-shaped tails, valvular nostrils, cutaneous respiration, elongated lungs, and salt glands, yet, knowledge on the genetic underpinnings of the transition remains limited. Herein, we report the first genome of Shaw’s sea snake (Hydrophis curtus) and use it to investigate sea snake secondary marine adaptation. A hybrid assembly strategy obtains a high-quality genome. Gene family analyses date a pulsed coding-gene expansion to ∼20 Ma, and these genes associate strongly with adaptations to marine environments. Analyses of selection pressure and convergent evolution discover the rapid evolution of protein-coding genes, and some convergent features. Additionally, 108 conserved noncoding elements appear to have evolved quickly, and these may underpin the phenotypic changes. Transposon elements may contribute to adaptive specializations by inserting into genomic regions around functionally related coding genes. The integration of genomic and transcriptomic analyses indicates independent origins and different components in sea snake and terrestrial snake venom; the venom gland of the sea snake harbors the highest PLA2 (17.23%) expression in selected elapids and these genes may organize tandemly in the genome. These analyses provide insights into the genetic mechanisms that underlay the secondary adaptation to marine and venom production of this sea snake.</description><subject>Adaptation, Biological</subject><subject>Animals</subject><subject>Aquatic Organisms</subject><subject>DNA Transposable Elements</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Genome</subject><subject>Hydrophiidae - genetics</subject><subject>Molecular Sequence Annotation</subject><subject>Multigene Family</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkE9PwjAYxhujEUSvHk2PcADatfvTIyEIJBgTwfPSde_CkLWz3TDc_Bp-PT-JI0Ovnt738Hue5PkhdE_JiBLBxoXZJ3AYF05KwtkF6lKfhUMaUnGJuiRsfk5Y1EE3zu0IoZwHwTXqMI-EoeC8i3abLeA5aFMANhleb-XH9-eXw2uQeK3lG-D-4phaU25zh1Vtq9oN8AscQO5PkDI6lfaIJ6ksK1nlRuPK4GXl8JO0uQY804fcGl2Arm7RVdak4O58e-j1cbaZLoar5_lyOlkNFQtENUyzkGS-9BkkYUQDBpRQEVDp-4JAmgaB8iLuCeVxCJhqZns8kmmUeEkURYpR1kP9tre05r0GV8VF7hTs91KDqV3sMV8w4XucNeioRZU1zlnI4tLmRTMopiQ--Y1bv_HZbxN4OHfXSQHpH_4rtAEGLWDq8r-yH3m7h7o</recordid><startdate>20200601</startdate><enddate>20200601</enddate><creator>Peng, Changjun</creator><creator>Ren, Jin-Long</creator><creator>Deng, Cao</creator><creator>Jiang, Dechun</creator><creator>Wang, Jichao</creator><creator>Qu, Jiangyong</creator><creator>Chang, Jiang</creator><creator>Yan, Chaochao</creator><creator>Jiang, Ke</creator><creator>Murphy, Robert W</creator><creator>Wu, Dong-Dong</creator><creator>Li, Jia-Tang</creator><general>Oxford University Press</general><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><orcidid>https://orcid.org/0000-0001-9823-9121</orcidid><orcidid>https://orcid.org/0000-0001-8117-2995</orcidid><orcidid>https://orcid.org/0000-0003-1799-194X</orcidid></search><sort><creationdate>20200601</creationdate><title>The Genome of Shaw’s Sea Snake (Hydrophis curtus) Reveals Secondary Adaptation to Its Marine Environment</title><author>Peng, Changjun ; Ren, Jin-Long ; Deng, Cao ; Jiang, Dechun ; Wang, Jichao ; Qu, Jiangyong ; Chang, Jiang ; Yan, Chaochao ; Jiang, Ke ; Murphy, Robert W ; Wu, Dong-Dong ; Li, Jia-Tang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c369t-df70f5a53eb78163e101961a5590edd66c28429c24e63caa0248ad8b2b888c313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adaptation, Biological</topic><topic>Animals</topic><topic>Aquatic Organisms</topic><topic>DNA Transposable Elements</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Genome</topic><topic>Hydrophiidae - genetics</topic><topic>Molecular Sequence Annotation</topic><topic>Multigene Family</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Peng, Changjun</creatorcontrib><creatorcontrib>Ren, Jin-Long</creatorcontrib><creatorcontrib>Deng, Cao</creatorcontrib><creatorcontrib>Jiang, Dechun</creatorcontrib><creatorcontrib>Wang, Jichao</creatorcontrib><creatorcontrib>Qu, Jiangyong</creatorcontrib><creatorcontrib>Chang, Jiang</creatorcontrib><creatorcontrib>Yan, Chaochao</creatorcontrib><creatorcontrib>Jiang, Ke</creatorcontrib><creatorcontrib>Murphy, Robert W</creatorcontrib><creatorcontrib>Wu, Dong-Dong</creatorcontrib><creatorcontrib>Li, Jia-Tang</creatorcontrib><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><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Peng, Changjun</au><au>Ren, Jin-Long</au><au>Deng, Cao</au><au>Jiang, Dechun</au><au>Wang, Jichao</au><au>Qu, Jiangyong</au><au>Chang, Jiang</au><au>Yan, Chaochao</au><au>Jiang, Ke</au><au>Murphy, Robert W</au><au>Wu, Dong-Dong</au><au>Li, Jia-Tang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Genome of Shaw’s Sea Snake (Hydrophis curtus) Reveals Secondary Adaptation to Its Marine Environment</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2020-06-01</date><risdate>2020</risdate><volume>37</volume><issue>6</issue><spage>1744</spage><epage>1760</epage><pages>1744-1760</pages><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>The transition of terrestrial snakes to marine life ∼10 Ma is ideal for exploring adaptive evolution. 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Transposon elements may contribute to adaptive specializations by inserting into genomic regions around functionally related coding genes. The integration of genomic and transcriptomic analyses indicates independent origins and different components in sea snake and terrestrial snake venom; the venom gland of the sea snake harbors the highest PLA2 (17.23%) expression in selected elapids and these genes may organize tandemly in the genome. These analyses provide insights into the genetic mechanisms that underlay the secondary adaptation to marine and venom production of this sea snake.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>32077944</pmid><doi>10.1093/molbev/msaa043</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-9823-9121</orcidid><orcidid>https://orcid.org/0000-0001-8117-2995</orcidid><orcidid>https://orcid.org/0000-0003-1799-194X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Biological Animals Aquatic Organisms DNA Transposable Elements Evolution, Molecular Female Genome Hydrophiidae - genetics Molecular Sequence Annotation Multigene Family |
title | The Genome of Shaw’s Sea Snake (Hydrophis curtus) Reveals Secondary Adaptation to Its Marine Environment |
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