The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda
Understanding the mechanisms that enforce, maintain or reverse the process of speciation is an important challenge in evolutionary biology. This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fus...
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Veröffentlicht in: | Molecular ecology 2019-01, Vol.28 (1), p.66-85 |
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description | Understanding the mechanisms that enforce, maintain or reverse the process of speciation is an important challenge in evolutionary biology. This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies from 18 sites spanning known genetic lineages and the four admixture zones between them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double‐digest restriction site‐associated DNA (ddRAD) SNPs to assess genome‐wide admixture, 16 microsatellites to provide continuity with published data and accurate biogeographic modelling, and a 491‐bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions impacted by the reorganization of Uganda's river networks that occurred during the formation of the West African Rift system over the last several hundred thousand years. Because tsetse fly population distributions are defined by rivers, admixture zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together. |
doi_str_mv | 10.1111/mec.14957 |
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This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies from 18 sites spanning known genetic lineages and the four admixture zones between them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double‐digest restriction site‐associated DNA (ddRAD) SNPs to assess genome‐wide admixture, 16 microsatellites to provide continuity with published data and accurate biogeographic modelling, and a 491‐bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions impacted by the reorganization of Uganda's river networks that occurred during the formation of the West African Rift system over the last several hundred thousand years. Because tsetse fly population distributions are defined by rivers, admixture zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together.</description><identifier>ISSN: 0962-1083</identifier><identifier>ISSN: 1365-294X</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.14957</identifier><identifier>PMID: 30471158</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Admixtures ; African rift system ; Animals ; Bayes Theorem ; Bayesian analysis ; Biological evolution ; Cytochrome ; Cytochrome oxidase I ; Cytochromes ; ddRAD ; Deoxyribonucleic acid ; Divergence ; DNA ; DNA, Mitochondrial - genetics ; Genetic analysis ; Genetic markers ; Genetic Speciation ; Genome, Insect - genetics ; Genomics ; Glossina fuscipes fuscipes ; Haplotypes - genetics ; Hybrid zones ; hybridization ; Hybridization, Genetic ; Maternal inheritance ; Metagenomics ; Microsatellite Repeats - genetics ; Microsatellites ; Mitochondria ; population genomics ; River networks ; Rivers ; Single-nucleotide polymorphism ; Speciation ; trypanosomiasis ; Tsetse Flies - genetics ; Tsetse Flies - pathogenicity ; Uganda - epidemiology ; vector</subject><ispartof>Molecular ecology, 2019-01, Vol.28 (1), p.66-85</ispartof><rights>2018 John Wiley & Sons Ltd</rights><rights>2018 John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4437-7bf92bdcd2d1d20a0a33d734a39f136b7d740769867f68db88a5bd79ecbcdfc53</citedby><cites>FETCH-LOGICAL-c4437-7bf92bdcd2d1d20a0a33d734a39f136b7d740769867f68db88a5bd79ecbcdfc53</cites><orcidid>0000-0003-2567-8013 ; 0000-0001-8974-0301</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.14957$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.14957$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30471158$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Saarman, Norah P.</creatorcontrib><creatorcontrib>Opiro, Robert</creatorcontrib><creatorcontrib>Hyseni, Chaz</creatorcontrib><creatorcontrib>Echodu, Richard</creatorcontrib><creatorcontrib>Opiyo, Elizabeth A.</creatorcontrib><creatorcontrib>Dion, Kirstin</creatorcontrib><creatorcontrib>Johnson, Thomas</creatorcontrib><creatorcontrib>Aksoy, Serap</creatorcontrib><creatorcontrib>Caccone, Adalgisa</creatorcontrib><title>The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Understanding the mechanisms that enforce, maintain or reverse the process of speciation is an important challenge in evolutionary biology. This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies from 18 sites spanning known genetic lineages and the four admixture zones between them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double‐digest restriction site‐associated DNA (ddRAD) SNPs to assess genome‐wide admixture, 16 microsatellites to provide continuity with published data and accurate biogeographic modelling, and a 491‐bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions impacted by the reorganization of Uganda's river networks that occurred during the formation of the West African Rift system over the last several hundred thousand years. Because tsetse fly population distributions are defined by rivers, admixture zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together.</description><subject>Admixtures</subject><subject>African rift system</subject><subject>Animals</subject><subject>Bayes Theorem</subject><subject>Bayesian analysis</subject><subject>Biological evolution</subject><subject>Cytochrome</subject><subject>Cytochrome oxidase I</subject><subject>Cytochromes</subject><subject>ddRAD</subject><subject>Deoxyribonucleic acid</subject><subject>Divergence</subject><subject>DNA</subject><subject>DNA, Mitochondrial - genetics</subject><subject>Genetic analysis</subject><subject>Genetic markers</subject><subject>Genetic Speciation</subject><subject>Genome, Insect - genetics</subject><subject>Genomics</subject><subject>Glossina fuscipes fuscipes</subject><subject>Haplotypes - genetics</subject><subject>Hybrid zones</subject><subject>hybridization</subject><subject>Hybridization, Genetic</subject><subject>Maternal inheritance</subject><subject>Metagenomics</subject><subject>Microsatellite Repeats - genetics</subject><subject>Microsatellites</subject><subject>Mitochondria</subject><subject>population genomics</subject><subject>River networks</subject><subject>Rivers</subject><subject>Single-nucleotide polymorphism</subject><subject>Speciation</subject><subject>trypanosomiasis</subject><subject>Tsetse Flies - genetics</subject><subject>Tsetse Flies - pathogenicity</subject><subject>Uganda - epidemiology</subject><subject>vector</subject><issn>0962-1083</issn><issn>1365-294X</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUFrFDEUx4Modq0e_AIS8NIepk0mmcnkIpSltkKLlxa8hUzysk3JJONkRl0_vbFbFxUaAnnwfvx4L3-E3lJyQss5HcCcUC4b8QytKGubqpb8y3O0IrKtK0o6doBe5XxPCGV107xEB4xwQWnTrRDc3AEe07gEPfsU8QZiGrzJODk8LGH2YwA8ZygXu7DFRxch5eyjxm7Jxo-Q98Ux1nbwP-ZlAvwzxdLxEd9udLT6NXrhdMjw5vE9RLcfz2_Wl9XV54tP67OrynDORCV6J-veGltbamuiiWbMCsY1k67s1QsrOBGt7Frh2s72Xaeb3goJpjfWmYYdog8777j0A1gDcZ50UOPkBz1tVdJe_duJ_k5t0jclW16TjhTB0aNgSl8XyLMafDYQgo6QlqxqygQXhMiuoO__Q-_TMsWyXqFaKYpP0kId7ygzlX-bwO2HoUT9Dk-V8NRDeIV99_f0e_JPWgU43QHffYDt0yZ1fb7eKX8BMX2l2A</recordid><startdate>201901</startdate><enddate>201901</enddate><creator>Saarman, Norah P.</creator><creator>Opiro, Robert</creator><creator>Hyseni, Chaz</creator><creator>Echodu, Richard</creator><creator>Opiyo, Elizabeth A.</creator><creator>Dion, Kirstin</creator><creator>Johnson, Thomas</creator><creator>Aksoy, Serap</creator><creator>Caccone, Adalgisa</creator><general>Blackwell Publishing Ltd</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>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2567-8013</orcidid><orcidid>https://orcid.org/0000-0001-8974-0301</orcidid></search><sort><creationdate>201901</creationdate><title>The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda</title><author>Saarman, Norah P. ; Opiro, Robert ; Hyseni, Chaz ; Echodu, Richard ; Opiyo, Elizabeth A. ; Dion, Kirstin ; Johnson, Thomas ; Aksoy, Serap ; Caccone, Adalgisa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4437-7bf92bdcd2d1d20a0a33d734a39f136b7d740769867f68db88a5bd79ecbcdfc53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Admixtures</topic><topic>African rift system</topic><topic>Animals</topic><topic>Bayes Theorem</topic><topic>Bayesian analysis</topic><topic>Biological evolution</topic><topic>Cytochrome</topic><topic>Cytochrome oxidase I</topic><topic>Cytochromes</topic><topic>ddRAD</topic><topic>Deoxyribonucleic acid</topic><topic>Divergence</topic><topic>DNA</topic><topic>DNA, Mitochondrial - genetics</topic><topic>Genetic analysis</topic><topic>Genetic markers</topic><topic>Genetic Speciation</topic><topic>Genome, Insect - genetics</topic><topic>Genomics</topic><topic>Glossina fuscipes fuscipes</topic><topic>Haplotypes - genetics</topic><topic>Hybrid zones</topic><topic>hybridization</topic><topic>Hybridization, Genetic</topic><topic>Maternal inheritance</topic><topic>Metagenomics</topic><topic>Microsatellite Repeats - genetics</topic><topic>Microsatellites</topic><topic>Mitochondria</topic><topic>population genomics</topic><topic>River networks</topic><topic>Rivers</topic><topic>Single-nucleotide polymorphism</topic><topic>Speciation</topic><topic>trypanosomiasis</topic><topic>Tsetse Flies - genetics</topic><topic>Tsetse Flies - pathogenicity</topic><topic>Uganda - epidemiology</topic><topic>vector</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Saarman, Norah P.</creatorcontrib><creatorcontrib>Opiro, Robert</creatorcontrib><creatorcontrib>Hyseni, Chaz</creatorcontrib><creatorcontrib>Echodu, Richard</creatorcontrib><creatorcontrib>Opiyo, Elizabeth A.</creatorcontrib><creatorcontrib>Dion, Kirstin</creatorcontrib><creatorcontrib>Johnson, Thomas</creatorcontrib><creatorcontrib>Aksoy, Serap</creatorcontrib><creatorcontrib>Caccone, Adalgisa</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</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>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Saarman, Norah P.</au><au>Opiro, Robert</au><au>Hyseni, Chaz</au><au>Echodu, Richard</au><au>Opiyo, Elizabeth A.</au><au>Dion, Kirstin</au><au>Johnson, Thomas</au><au>Aksoy, Serap</au><au>Caccone, Adalgisa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2019-01</date><risdate>2019</risdate><volume>28</volume><issue>1</issue><spage>66</spage><epage>85</epage><pages>66-85</pages><issn>0962-1083</issn><issn>1365-294X</issn><eissn>1365-294X</eissn><abstract>Understanding the mechanisms that enforce, maintain or reverse the process of speciation is an important challenge in evolutionary biology. This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies from 18 sites spanning known genetic lineages and the four admixture zones between them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double‐digest restriction site‐associated DNA (ddRAD) SNPs to assess genome‐wide admixture, 16 microsatellites to provide continuity with published data and accurate biogeographic modelling, and a 491‐bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions impacted by the reorganization of Uganda's river networks that occurred during the formation of the West African Rift system over the last several hundred thousand years. Because tsetse fly population distributions are defined by rivers, admixture zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>30471158</pmid><doi>10.1111/mec.14957</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0003-2567-8013</orcidid><orcidid>https://orcid.org/0000-0001-8974-0301</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Admixtures African rift system Animals Bayes Theorem Bayesian analysis Biological evolution Cytochrome Cytochrome oxidase I Cytochromes ddRAD Deoxyribonucleic acid Divergence DNA DNA, Mitochondrial - genetics Genetic analysis Genetic markers Genetic Speciation Genome, Insect - genetics Genomics Glossina fuscipes fuscipes Haplotypes - genetics Hybrid zones hybridization Hybridization, Genetic Maternal inheritance Metagenomics Microsatellite Repeats - genetics Microsatellites Mitochondria population genomics River networks Rivers Single-nucleotide polymorphism Speciation trypanosomiasis Tsetse Flies - genetics Tsetse Flies - pathogenicity Uganda - epidemiology vector |
title | The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda |
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