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Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals
Abstract Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether livi...
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Published in: | Molecular biology and evolution 2019-10, Vol.36 (10), p.2171-2183 |
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description | Abstract
Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets. |
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Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msz127</identifier><identifier>PMID: 31311032</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Biological Evolution ; Chiroptera - genetics ; Chiroptera - metabolism ; Diet ; Discoveries ; Trehalase - genetics ; Trehalase - metabolism</subject><ispartof>Molecular biology and evolution, 2019-10, Vol.36 (10), p.2171-2183</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2019</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c420t-1b5120fb63f4881df429e18e516f16b4e6ceb2b0a11137da571ab5cdaa3f1ea3</citedby><cites>FETCH-LOGICAL-c420t-1b5120fb63f4881df429e18e516f16b4e6ceb2b0a11137da571ab5cdaa3f1ea3</cites><orcidid>0000-0002-0951-0432 ; 0000-0002-7848-6392</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/PMC6759077/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6759077/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,1604,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31311032$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Satta, Yoko</contributor><creatorcontrib>Jiao, Hengwu</creatorcontrib><creatorcontrib>Zhang, Libiao</creatorcontrib><creatorcontrib>Xie, Huan-Wang</creatorcontrib><creatorcontrib>Simmons, Nancy B</creatorcontrib><creatorcontrib>Liu, Hui</creatorcontrib><creatorcontrib>Zhao, Huabin</creatorcontrib><title>Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract
Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.</description><subject>Animals</subject><subject>Biological Evolution</subject><subject>Chiroptera - genetics</subject><subject>Chiroptera - metabolism</subject><subject>Diet</subject><subject>Discoveries</subject><subject>Trehalase - genetics</subject><subject>Trehalase - metabolism</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqFkb1P5DAQxS10CPaAkvbk8pqAx47jpEFCfOwhsaJge2uSHYNREu_ZyUp3fz1By2dF9Uaap98bzWPsGMQJiEqddqGtaXPapf8gzQ6bgVYmAwPVDzYTZppzocp99jOlJyEgz4tij-0rUABCyRlbLCM9YouJ-Jx64pg48kVoqRlbjPzeP_Q4jJF4cPzS04Dx36Qbisk73-DgQ899zxfYddimQ7brJqGjVz1gy-ur5cWf7PZufnNxfps1uRRDBrUGKVxdKJeXJaxcLiuCkjQUDoo6p6KhWtYCAUCZFWoDWOtmhagcEKoDdrbFrse6o1VD_RCxtevou-k-G9Dbr5veP9qHsLGF0ZUwZgL8fgXE8HekNNjOp4baFnsKY7JS6kpppWU5WbOttYkhpUjuPQaEfWnAbhuw2wYm_6_Pt727317-kR3G9TesZ7SDk4E</recordid><startdate>20191001</startdate><enddate>20191001</enddate><creator>Jiao, Hengwu</creator><creator>Zhang, Libiao</creator><creator>Xie, Huan-Wang</creator><creator>Simmons, Nancy B</creator><creator>Liu, Hui</creator><creator>Zhao, Huabin</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/0000-0002-0951-0432</orcidid><orcidid>https://orcid.org/0000-0002-7848-6392</orcidid></search><sort><creationdate>20191001</creationdate><title>Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals</title><author>Jiao, Hengwu ; Zhang, Libiao ; Xie, Huan-Wang ; Simmons, Nancy B ; Liu, Hui ; Zhao, Huabin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c420t-1b5120fb63f4881df429e18e516f16b4e6ceb2b0a11137da571ab5cdaa3f1ea3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Biological Evolution</topic><topic>Chiroptera - genetics</topic><topic>Chiroptera - metabolism</topic><topic>Diet</topic><topic>Discoveries</topic><topic>Trehalase - genetics</topic><topic>Trehalase - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiao, Hengwu</creatorcontrib><creatorcontrib>Zhang, Libiao</creatorcontrib><creatorcontrib>Xie, Huan-Wang</creatorcontrib><creatorcontrib>Simmons, Nancy B</creatorcontrib><creatorcontrib>Liu, Hui</creatorcontrib><creatorcontrib>Zhao, Huabin</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>Jiao, Hengwu</au><au>Zhang, Libiao</au><au>Xie, Huan-Wang</au><au>Simmons, Nancy B</au><au>Liu, Hui</au><au>Zhao, Huabin</au><au>Satta, Yoko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2019-10-01</date><risdate>2019</risdate><volume>36</volume><issue>10</issue><spage>2171</spage><epage>2183</epage><pages>2171-2183</pages><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>31311032</pmid><doi>10.1093/molbev/msz127</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0951-0432</orcidid><orcidid>https://orcid.org/0000-0002-7848-6392</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biological Evolution Chiroptera - genetics Chiroptera - metabolism Diet Discoveries Trehalase - genetics Trehalase - metabolism |
title | Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals |
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