Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population
In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Ni...
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description | In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10-20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions. |
doi_str_mv | 10.1371/journal.pgen.1002504 |
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An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10-20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1002504</identifier><identifier>PMID: 22396655</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal genetics ; Animals ; Biological Evolution ; Biology ; Biomedical research ; Chimpanzees ; DNA, Mitochondrial - genetics ; Evolution ; Evolutionary biology ; Genealogy ; Genetic aspects ; Genetic Speciation ; Genetic testing ; Genetic Variation ; Genetics ; Genome ; Genomics ; Haplotypes ; Mitochondrial DNA ; Monkeys & apes ; Pan troglodytes ; Physiological aspects ; Polymorphism, Single Nucleotide ; Population ; Population Dynamics ; Population genetics ; Rivers ; Sequence Analysis, DNA</subject><ispartof>PLoS genetics, 2012-03, Vol.8 (3), p.e1002504-e1002504</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Bowden et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bowden R, MacFie TS, Myers S, Hellenthal G, Nerrienet E, et al. (2012) Genomic Tools for Evolution and Conservation in the Chimpanzee: Pan troglodytes ellioti Is a Genetically Distinct Population. PLoS Genet 8(3): e1002504. doi:10.1371/journal.pgen.1002504</rights><rights>Bowden et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-5b6dd320f65856370b46face3377a8c269cf34343d4d87bea11447d35b073c043</citedby><cites>FETCH-LOGICAL-c725t-5b6dd320f65856370b46face3377a8c269cf34343d4d87bea11447d35b073c043</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3291532/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3291532/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22396655$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Worobey, Michael</contributor><creatorcontrib>Bowden, Rory</creatorcontrib><creatorcontrib>MacFie, Tammie S</creatorcontrib><creatorcontrib>Myers, Simon</creatorcontrib><creatorcontrib>Hellenthal, Garrett</creatorcontrib><creatorcontrib>Nerrienet, Eric</creatorcontrib><creatorcontrib>Bontrop, Ronald E</creatorcontrib><creatorcontrib>Freeman, Colin</creatorcontrib><creatorcontrib>Donnelly, Peter</creatorcontrib><creatorcontrib>Mundy, Nicholas I</creatorcontrib><title>Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10-20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.</description><subject>Animal genetics</subject><subject>Animals</subject><subject>Biological Evolution</subject><subject>Biology</subject><subject>Biomedical research</subject><subject>Chimpanzees</subject><subject>DNA, Mitochondrial - genetics</subject><subject>Evolution</subject><subject>Evolutionary biology</subject><subject>Genealogy</subject><subject>Genetic aspects</subject><subject>Genetic Speciation</subject><subject>Genetic testing</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genome</subject><subject>Genomics</subject><subject>Haplotypes</subject><subject>Mitochondrial DNA</subject><subject>Monkeys & apes</subject><subject>Pan troglodytes</subject><subject>Physiological aspects</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Population</subject><subject>Population Dynamics</subject><subject>Population genetics</subject><subject>Rivers</subject><subject>Sequence Analysis, DNA</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk99vFCEQxzdGY2v1PzBKYqLx4U5YYGF9MGkarZc01vjrlXAwe0fDwXVhG2v84-V626Zn-qDhARg-851hYKrqKcFTQgV5cxaHPmg_XS8gTAnGNcfsXrVPOKcTwTC7f2u9Vz1K6QxjymUrHlZ7dU3bpuF8v_p9DCGunEE5Rp9QF3sEF9EP2cWAdLDIxJCgv9BXBhdQXgIyS7da6_AL4C36rIutjwsf7WWGhMB7F7NDLiGNSmqQndHeXyLrUnbBZLSO68Ff6T2uHnTaJ3gyzgfV9w_vvx19nJycHs-ODk8mRtQ8T_i8sZbWuGu45A0VeM6aThugVAgtTd20pqOsDMusFHPQhDAmLOVzLKjBjB5Uz7e6ax-TGguXFKGEciwxaQsx2xI26jO17t1K95cqaqeuDLFfKN2Xm3hQEtMOmCSaWWCc1NJizBra4nnZ2NYWrXdjtGG-Amsg5F77HdHdk-CWahEvFK1bwmldBF6NAn08HyBltXLJlMLqAHFIqq0bKaTEspAv_iLvvtxILXTJ34UulrBmo6kOaylK6oJutKZ3UGVYKP8jBuhcse84vN5xKEyGn3mhh5TU7OuX_2A__Tt7-mOXfXmLXYL2eZnG75t2QbYFTR9T6qG7eQ-C1aafriunNv2kxn4qbs9uv-WN03UD0T8O7Bq6</recordid><startdate>20120301</startdate><enddate>20120301</enddate><creator>Bowden, Rory</creator><creator>MacFie, Tammie S</creator><creator>Myers, Simon</creator><creator>Hellenthal, Garrett</creator><creator>Nerrienet, Eric</creator><creator>Bontrop, Ronald E</creator><creator>Freeman, Colin</creator><creator>Donnelly, Peter</creator><creator>Mundy, Nicholas I</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120301</creationdate><title>Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population</title><author>Bowden, Rory ; MacFie, Tammie S ; Myers, Simon ; Hellenthal, Garrett ; Nerrienet, Eric ; Bontrop, Ronald E ; Freeman, Colin ; Donnelly, Peter ; Mundy, Nicholas I</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c725t-5b6dd320f65856370b46face3377a8c269cf34343d4d87bea11447d35b073c043</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animal genetics</topic><topic>Animals</topic><topic>Biological Evolution</topic><topic>Biology</topic><topic>Biomedical research</topic><topic>Chimpanzees</topic><topic>DNA, Mitochondrial - genetics</topic><topic>Evolution</topic><topic>Evolutionary biology</topic><topic>Genealogy</topic><topic>Genetic aspects</topic><topic>Genetic Speciation</topic><topic>Genetic testing</topic><topic>Genetic Variation</topic><topic>Genetics</topic><topic>Genome</topic><topic>Genomics</topic><topic>Haplotypes</topic><topic>Mitochondrial DNA</topic><topic>Monkeys & apes</topic><topic>Pan troglodytes</topic><topic>Physiological aspects</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Population</topic><topic>Population Dynamics</topic><topic>Population genetics</topic><topic>Rivers</topic><topic>Sequence Analysis, DNA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bowden, Rory</creatorcontrib><creatorcontrib>MacFie, Tammie S</creatorcontrib><creatorcontrib>Myers, Simon</creatorcontrib><creatorcontrib>Hellenthal, Garrett</creatorcontrib><creatorcontrib>Nerrienet, Eric</creatorcontrib><creatorcontrib>Bontrop, Ronald E</creatorcontrib><creatorcontrib>Freeman, Colin</creatorcontrib><creatorcontrib>Donnelly, Peter</creatorcontrib><creatorcontrib>Mundy, Nicholas I</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bowden, Rory</au><au>MacFie, Tammie S</au><au>Myers, Simon</au><au>Hellenthal, Garrett</au><au>Nerrienet, Eric</au><au>Bontrop, Ronald E</au><au>Freeman, Colin</au><au>Donnelly, Peter</au><au>Mundy, Nicholas I</au><au>Worobey, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2012-03-01</date><risdate>2012</risdate><volume>8</volume><issue>3</issue><spage>e1002504</spage><epage>e1002504</epage><pages>e1002504-e1002504</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10-20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22396655</pmid><doi>10.1371/journal.pgen.1002504</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animal genetics Animals Biological Evolution Biology Biomedical research Chimpanzees DNA, Mitochondrial - genetics Evolution Evolutionary biology Genealogy Genetic aspects Genetic Speciation Genetic testing Genetic Variation Genetics Genome Genomics Haplotypes Mitochondrial DNA Monkeys & apes Pan troglodytes Physiological aspects Polymorphism, Single Nucleotide Population Population Dynamics Population genetics Rivers Sequence Analysis, DNA |
title | Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population |
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