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Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur
Understanding the frequency, spatiotemporal dynamics and impacts of parasite coinfections is fundamental to developing control measures and predicting disease impacts. The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by...
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Published in: | Molecular ecology 2022-05, Vol.31 (9), p.2730-2751 |
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creator | Thomas, Rebecca C. Dunn, Jenny C. Dawson, Deborah A. Hipperson, Helen Horsburgh, Gavin J. Morris, Antony J. Orsman, Chris Mallord, John Grice, Philip V. Hamer, Keith C. Eraud, Cyril Hervé, Lormée Goodman, Simon J. |
description | Understanding the frequency, spatiotemporal dynamics and impacts of parasite coinfections is fundamental to developing control measures and predicting disease impacts. The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high‐throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron‐hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%–100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within‐host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite‐induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations. |
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The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high‐throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron‐hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%–100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within‐host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite‐induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.16421</identifier><identifier>PMID: 35253301</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Bird Diseases - epidemiology ; Bird Diseases - parasitology ; coinfection ; Coinfection - veterinary ; Columbidae - parasitology ; Disease control ; Epidemiology ; Haemosporida ; haemosporidians ; high‐throughput sequencing ; Hydrogenase ; Immunomodulation ; Impact prediction ; Infections ; Life span ; Longitudinal studies ; Natural populations ; next‐generation sequencing ; NGS ; Original ; ORIGINAL ARTICLES ; Parasites ; Populations ; Predictive control ; Streptopelia turtur ; Threatened species ; Trichomonas - genetics ; Trichomonas gallinae ; Turtles</subject><ispartof>Molecular ecology, 2022-05, Vol.31 (9), p.2730-2751</ispartof><rights>2022 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high‐throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron‐hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%–100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within‐host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite‐induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.</description><subject>Animals</subject><subject>Bird Diseases - epidemiology</subject><subject>Bird Diseases - parasitology</subject><subject>coinfection</subject><subject>Coinfection - veterinary</subject><subject>Columbidae - parasitology</subject><subject>Disease control</subject><subject>Epidemiology</subject><subject>Haemosporida</subject><subject>haemosporidians</subject><subject>high‐throughput sequencing</subject><subject>Hydrogenase</subject><subject>Immunomodulation</subject><subject>Impact prediction</subject><subject>Infections</subject><subject>Life span</subject><subject>Longitudinal studies</subject><subject>Natural populations</subject><subject>next‐generation sequencing</subject><subject>NGS</subject><subject>Original</subject><subject>ORIGINAL ARTICLES</subject><subject>Parasites</subject><subject>Populations</subject><subject>Predictive control</subject><subject>Streptopelia turtur</subject><subject>Threatened species</subject><subject>Trichomonas - genetics</subject><subject>Trichomonas gallinae</subject><subject>Turtles</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1ks1u1DAQgCMEokvhwAsgS1zgkNY_iZtwQKpWS1upiAMgcbMmzmTXVWIH2wnqI_GWOE2pAAlfbHk-f56xJ8teMnrC0jgdUJ8wWXD2KNswIcuc18W3x9mG1pLnjFbiKHsWwg2lTPCyfJodiZKXQlC2yX6eh4AhGLsnHiIG4joygodgIhLtjO1QR-MsAduSMEJaRxxG56EnIXowlszgDdwxswEyYIQGvHZtcr4jVzaY_SEG0jlP4mFx2oB-Xg-ky3aTdyOCJXHysUfSujll8Tl6HGMK9Em5RCb_PHvSQR_wxf18nH39sPuyvcyvP11cbc-vc10UguWcnTWtrOoKOXCuuQbEtkShsexS9SlQdU3dyhLTvhRNxcuCsa4D7IBqLMRx9n71jlMzYKvRpjJ7NXozgL9VDoz6O2LNQe3drOrlcfkieHMv8O77hCGqwQSNfQ8W3RQUl0JWZ7KoRUJf_4PeuMnbVF6iykJQWlGZqLcrpb0LwWP3kAyjamkAlRpA3TVAYl_9mf0D-fvHE3C6Aj9Mj7f_N6mPu-2q_AWtysEK</recordid><startdate>202205</startdate><enddate>202205</enddate><creator>Thomas, Rebecca C.</creator><creator>Dunn, Jenny C.</creator><creator>Dawson, Deborah A.</creator><creator>Hipperson, Helen</creator><creator>Horsburgh, Gavin J.</creator><creator>Morris, Antony J.</creator><creator>Orsman, Chris</creator><creator>Mallord, John</creator><creator>Grice, Philip V.</creator><creator>Hamer, Keith C.</creator><creator>Eraud, Cyril</creator><creator>Hervé, Lormée</creator><creator>Goodman, Simon J.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>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/0000-0002-6277-2781</orcidid><orcidid>https://orcid.org/0000-0003-1517-9835</orcidid><orcidid>https://orcid.org/0000-0003-4118-8575</orcidid></search><sort><creationdate>202205</creationdate><title>Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur</title><author>Thomas, Rebecca C. ; 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The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high‐throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron‐hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%–100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within‐host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite‐induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35253301</pmid><doi>10.1111/mec.16421</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0002-6277-2781</orcidid><orcidid>https://orcid.org/0000-0003-1517-9835</orcidid><orcidid>https://orcid.org/0000-0003-4118-8575</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bird Diseases - epidemiology Bird Diseases - parasitology coinfection Coinfection - veterinary Columbidae - parasitology Disease control Epidemiology Haemosporida haemosporidians high‐throughput sequencing Hydrogenase Immunomodulation Impact prediction Infections Life span Longitudinal studies Natural populations next‐generation sequencing NGS Original ORIGINAL ARTICLES Parasites Populations Predictive control Streptopelia turtur Threatened species Trichomonas - genetics Trichomonas gallinae Turtles |
title | Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur |
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