hearing gene Prestin reunites echolocating bats
The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encod...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2008-09, Vol.105 (37), p.13959-13964 |
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description | The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encoded by the gene PRESTIN: Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence. |
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This process is driven by the recently discovered protein prestin, encoded by the gene PRESTIN: Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0802097105</identifier><identifier>PMID: 18776049</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Acoustic echoes ; Animal communication ; Animals ; Anion Transport Proteins - genetics ; Anion Transport Proteins - metabolism ; Bats ; Biological Sciences ; Biological taxonomies ; Cells ; Chiroptera - genetics ; Chiroptera - physiology ; Cochlea ; Echolocation - physiology ; Evolution ; Evolution & development ; Genes ; Hearing - genetics ; Hearing - physiology ; Humans ; Mammals ; Molecular Sequence Data ; Outer hair cells ; Phylogenetics ; Phylogeny ; Positive selection ; Proteins</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2008-09, Vol.105 (37), p.13959-13964</ispartof><rights>Copyright 2008 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Sep 16, 2008</rights><rights>2008 by The National Academy of Sciences of the USA</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c554t-f4c8599692d4e2712fd06175d23d1f02c9568988c2176c391c5b7c8e765bb3973</citedby><cites>FETCH-LOGICAL-c554t-f4c8599692d4e2712fd06175d23d1f02c9568988c2176c391c5b7c8e765bb3973</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/105/37.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25464158$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25464158$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,728,781,785,804,886,27929,27930,53796,53798,58022,58255</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18776049$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Gang</creatorcontrib><creatorcontrib>Wang, Jinhong</creatorcontrib><creatorcontrib>Rossiter, Stephen J</creatorcontrib><creatorcontrib>Jones, Gareth</creatorcontrib><creatorcontrib>Cotton, James A</creatorcontrib><creatorcontrib>Zhang, Shuyi</creatorcontrib><title>hearing gene Prestin reunites echolocating bats</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encoded by the gene PRESTIN: Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence.</description><subject>Acoustic echoes</subject><subject>Animal communication</subject><subject>Animals</subject><subject>Anion Transport Proteins - genetics</subject><subject>Anion Transport Proteins - metabolism</subject><subject>Bats</subject><subject>Biological Sciences</subject><subject>Biological taxonomies</subject><subject>Cells</subject><subject>Chiroptera - genetics</subject><subject>Chiroptera - physiology</subject><subject>Cochlea</subject><subject>Echolocation - physiology</subject><subject>Evolution</subject><subject>Evolution & development</subject><subject>Genes</subject><subject>Hearing - genetics</subject><subject>Hearing - physiology</subject><subject>Humans</subject><subject>Mammals</subject><subject>Molecular Sequence Data</subject><subject>Outer hair cells</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Positive selection</subject><subject>Proteins</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0U1vEzEQBmALgWgonDkBKw5IHLaZ8bcvlVBFAakSSNCz5fV6k40262DvovLvcZSoAS49-TDPvPLMEPIS4QJBseVudPkCNFAwCkE8IgsEg7XkBh6TBQBVteaUn5FnOW8AwAgNT8kZaqUkcLMgy3VwqR9X1SqMofqWQp76sUphHvsp5Cr4dRyid9OeNG7Kz8mTzg05vDi-5-T2-uOPq8_1zddPX64-3NReCD7VHfdaGCMNbXmgCmnXgkQlWspa7IB6I6Q2WnuKSnpm0ItGeR2UFE3DjGLn5PKQu5ubbWh9GKfkBrtL_dal3za63v5bGfu1XcVflgrOhcQS8O4YkOLPuYxlt332YRjcGOKcrSw_oFLwByEFygEVFPj2P7iJcxrLFopBqjkwWtDygHyKOafQ3X8Zwe5PZvcns6eTlY7Xf0968scbFfD-CPadpzhhmbLIjDC2m4dhCndTsdUDtpBXB7LJU0z3puxNchS61N8c6p2L1q1Sn-3t9zIgAxRlRIPsD6B7u9I</recordid><startdate>20080916</startdate><enddate>20080916</enddate><creator>Li, Gang</creator><creator>Wang, Jinhong</creator><creator>Rossiter, Stephen J</creator><creator>Jones, Gareth</creator><creator>Cotton, James A</creator><creator>Zhang, Shuyi</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20080916</creationdate><title>hearing gene Prestin reunites echolocating bats</title><author>Li, Gang ; Wang, Jinhong ; Rossiter, Stephen J ; Jones, Gareth ; Cotton, James A ; Zhang, Shuyi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c554t-f4c8599692d4e2712fd06175d23d1f02c9568988c2176c391c5b7c8e765bb3973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Acoustic echoes</topic><topic>Animal communication</topic><topic>Animals</topic><topic>Anion Transport Proteins - genetics</topic><topic>Anion Transport Proteins - metabolism</topic><topic>Bats</topic><topic>Biological Sciences</topic><topic>Biological taxonomies</topic><topic>Cells</topic><topic>Chiroptera - genetics</topic><topic>Chiroptera - physiology</topic><topic>Cochlea</topic><topic>Echolocation - physiology</topic><topic>Evolution</topic><topic>Evolution & development</topic><topic>Genes</topic><topic>Hearing - genetics</topic><topic>Hearing - physiology</topic><topic>Humans</topic><topic>Mammals</topic><topic>Molecular Sequence Data</topic><topic>Outer hair cells</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Positive selection</topic><topic>Proteins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Gang</creatorcontrib><creatorcontrib>Wang, Jinhong</creatorcontrib><creatorcontrib>Rossiter, Stephen J</creatorcontrib><creatorcontrib>Jones, Gareth</creatorcontrib><creatorcontrib>Cotton, James A</creatorcontrib><creatorcontrib>Zhang, Shuyi</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Gang</au><au>Wang, Jinhong</au><au>Rossiter, Stephen J</au><au>Jones, Gareth</au><au>Cotton, James A</au><au>Zhang, Shuyi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>hearing gene Prestin reunites echolocating bats</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2008-09-16</date><risdate>2008</risdate><volume>105</volume><issue>37</issue><spage>13959</spage><epage>13964</epage><pages>13959-13964</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encoded by the gene PRESTIN: Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>18776049</pmid><doi>10.1073/pnas.0802097105</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic echoes Animal communication Animals Anion Transport Proteins - genetics Anion Transport Proteins - metabolism Bats Biological Sciences Biological taxonomies Cells Chiroptera - genetics Chiroptera - physiology Cochlea Echolocation - physiology Evolution Evolution & development Genes Hearing - genetics Hearing - physiology Humans Mammals Molecular Sequence Data Outer hair cells Phylogenetics Phylogeny Positive selection Proteins |
title | hearing gene Prestin reunites echolocating bats |
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