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Virulence Evolution via Pleiotropy in Vector‐Borne Plant Pathogens
ABSTRACT The dynamics of virulence evolution in vector‐borne plant pathogens can be complex. Here, we use individual‐based, quantitative‐genetic simulations to investigate how virulence evolution depends on genetic trade‐offs and population structure. Although quite generic, the model is inspired by...
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Published in: | Ecology and evolution 2024-12, Vol.14 (12), p.e70741-n/a |
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The dynamics of virulence evolution in vector‐borne plant pathogens can be complex. Here, we use individual‐based, quantitative‐genetic simulations to investigate how virulence evolution depends on genetic trade‐offs and population structure. Although quite generic, the model is inspired by the ecology of the plant‐pathogenic bacterium Xylella fastidiosa, and we use it to gain insights into possible modes of virulence evolution in that group. In particular, we aim to sharpen our intuition about how virulence may evolve over short time scales via antagonistically pleiotropic alleles affecting pathogen performance within hosts and vectors. We find that even when pathogens find themselves much more often in hosts than vectors, selection in the vector environment can cause correlational and potentially non‐adaptive changes in virulence in the host. The extent of such correlational virulence evolution depends on many system parameters, including the pathogen transmission rate, the proportion of the pathogen population occurring in hosts, the strengths of selection in host and vector environments, and the functional relationship between pathogen load and virulence. But there is a statistical interaction between the strength of selection in vectors and the proportion of the pathogen population in hosts, such that if within‐vector selection is strong enough, over the short term, it can dominate virulence evolution, even when the host environment predominates.
In general, natural selection is more efficient in more commonly encountered habitats. Here, with evolutionary simulations, we show that even when vector‐borne pathogens much more often occur within hosts, correlational and potentially maladaptive virulence evolution can be driven by selection in vectors. |
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The dynamics of virulence evolution in vector‐borne plant pathogens can be complex. Here, we use individual‐based, quantitative‐genetic simulations to investigate how virulence evolution depends on genetic trade‐offs and population structure. Although quite generic, the model is inspired by the ecology of the plant‐pathogenic bacterium Xylella fastidiosa, and we use it to gain insights into possible modes of virulence evolution in that group. In particular, we aim to sharpen our intuition about how virulence may evolve over short time scales via antagonistically pleiotropic alleles affecting pathogen performance within hosts and vectors. We find that even when pathogens find themselves much more often in hosts than vectors, selection in the vector environment can cause correlational and potentially non‐adaptive changes in virulence in the host. The extent of such correlational virulence evolution depends on many system parameters, including the pathogen transmission rate, the proportion of the pathogen population occurring in hosts, the strengths of selection in host and vector environments, and the functional relationship between pathogen load and virulence. But there is a statistical interaction between the strength of selection in vectors and the proportion of the pathogen population in hosts, such that if within‐vector selection is strong enough, over the short term, it can dominate virulence evolution, even when the host environment predominates.
In general, natural selection is more efficient in more commonly encountered habitats. Here, with evolutionary simulations, we show that even when vector‐borne pathogens much more often occur within hosts, correlational and potentially maladaptive virulence evolution can be driven by selection in vectors.</description><identifier>ISSN: 2045-7758</identifier><identifier>EISSN: 2045-7758</identifier><identifier>DOI: 10.1002/ece3.70741</identifier><identifier>PMID: 39687580</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Adaptive systems ; Agroecology ; Applied Ecology ; Disease Ecology ; Disease transmission ; Dynamic structural analysis ; Equilibrium ; Evolution ; Evolution & development ; Evolutionary Ecology ; Genomes ; Genotype & phenotype ; Habitats ; Microbial Ecology ; Mortality ; Mutation ; Normal distribution ; Parasitology ; Pathogens ; Pleiotropy ; Population (statistical) ; Population Genetics ; Population structure ; Quantitative Genetics ; Simulation ; Vectors ; Vectors (Biology) ; Virulence</subject><ispartof>Ecology and evolution, 2024-12, Vol.14 (12), p.e70741-n/a</ispartof><rights>2024 The Author(s). published by John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Ecology and Evolution published by John Wiley & Sons Ltd.</rights><rights>2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3551-1c38dc91b530e252855beb062588d06f96d533b8b0c9d6b84e008b1ebaf1b5f33</cites><orcidid>0000-0001-6133-7086</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3149459687/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3149459687?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,11561,25752,27923,27924,37011,37012,44589,46051,46475,53790,53792,74997</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39687580$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Woodruff, Elise</creatorcontrib><creatorcontrib>Hardy, Nate B.</creatorcontrib><title>Virulence Evolution via Pleiotropy in Vector‐Borne Plant Pathogens</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>ABSTRACT
The dynamics of virulence evolution in vector‐borne plant pathogens can be complex. Here, we use individual‐based, quantitative‐genetic simulations to investigate how virulence evolution depends on genetic trade‐offs and population structure. Although quite generic, the model is inspired by the ecology of the plant‐pathogenic bacterium Xylella fastidiosa, and we use it to gain insights into possible modes of virulence evolution in that group. In particular, we aim to sharpen our intuition about how virulence may evolve over short time scales via antagonistically pleiotropic alleles affecting pathogen performance within hosts and vectors. We find that even when pathogens find themselves much more often in hosts than vectors, selection in the vector environment can cause correlational and potentially non‐adaptive changes in virulence in the host. The extent of such correlational virulence evolution depends on many system parameters, including the pathogen transmission rate, the proportion of the pathogen population occurring in hosts, the strengths of selection in host and vector environments, and the functional relationship between pathogen load and virulence. But there is a statistical interaction between the strength of selection in vectors and the proportion of the pathogen population in hosts, such that if within‐vector selection is strong enough, over the short term, it can dominate virulence evolution, even when the host environment predominates.
In general, natural selection is more efficient in more commonly encountered habitats. Here, with evolutionary simulations, we show that even when vector‐borne pathogens much more often occur within hosts, correlational and potentially maladaptive virulence evolution can be driven by selection in vectors.</description><subject>Adaptive systems</subject><subject>Agroecology</subject><subject>Applied Ecology</subject><subject>Disease Ecology</subject><subject>Disease transmission</subject><subject>Dynamic structural analysis</subject><subject>Equilibrium</subject><subject>Evolution</subject><subject>Evolution & development</subject><subject>Evolutionary Ecology</subject><subject>Genomes</subject><subject>Genotype & phenotype</subject><subject>Habitats</subject><subject>Microbial Ecology</subject><subject>Mortality</subject><subject>Mutation</subject><subject>Normal distribution</subject><subject>Parasitology</subject><subject>Pathogens</subject><subject>Pleiotropy</subject><subject>Population (statistical)</subject><subject>Population Genetics</subject><subject>Population structure</subject><subject>Quantitative Genetics</subject><subject>Simulation</subject><subject>Vectors</subject><subject>Vectors (Biology)</subject><subject>Virulence</subject><issn>2045-7758</issn><issn>2045-7758</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9kUFPHCEUx4mpqcZ66Qcwk_TSNFkLw8DAqbHrtpqY6KH1SoB5s7KZhRVm1uytH6GfsZ-krKNGPcgFwvvx4-X9EfpI8DHBuPwKFuhxjeuK7KD9EldsUtdMvHt23kOHKS1wXhyXFa7foz0qucgVvI9Or10cOvAWitk6dEPvgi_WThdXHbjQx7DaFM4X12D7EP_9-fs9RA-5qH1fXOn-JszBpw9ot9VdgsOH_QD9_jH7NT2bXFz-PJ-eXEwsZYxMiKWisZIYRjGUrBSMGTCYl0yIBvNW8oZRaoTBVjbciAowFoaA0W1-01J6gM5HbxP0Qq2iW-q4UUE7dX8R4lzp2DvbgYL8ESW0kcxCZUVrBAhKpWkaMKS2dXZ9G12rwSwzDb6PunshfVnx7kbNw1oRwisuKc-Gzw-GGG4HSL1aumShy7OBMCRFSeaI4JXM6KdX6CIM0edZbSlZsW0emfoyUjaGlCK0T90QrLZhq23Y6j7sDB897_8JfYw2A2QE7lwHmzdUajad0VH6H9aetI0</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Woodruff, Elise</creator><creator>Hardy, Nate B.</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7X2</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6133-7086</orcidid></search><sort><creationdate>202412</creationdate><title>Virulence Evolution via Pleiotropy in Vector‐Borne Plant Pathogens</title><author>Woodruff, Elise ; Hardy, Nate B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3551-1c38dc91b530e252855beb062588d06f96d533b8b0c9d6b84e008b1ebaf1b5f33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adaptive systems</topic><topic>Agroecology</topic><topic>Applied Ecology</topic><topic>Disease Ecology</topic><topic>Disease transmission</topic><topic>Dynamic structural analysis</topic><topic>Equilibrium</topic><topic>Evolution</topic><topic>Evolution & development</topic><topic>Evolutionary Ecology</topic><topic>Genomes</topic><topic>Genotype & phenotype</topic><topic>Habitats</topic><topic>Microbial Ecology</topic><topic>Mortality</topic><topic>Mutation</topic><topic>Normal distribution</topic><topic>Parasitology</topic><topic>Pathogens</topic><topic>Pleiotropy</topic><topic>Population (statistical)</topic><topic>Population Genetics</topic><topic>Population structure</topic><topic>Quantitative Genetics</topic><topic>Simulation</topic><topic>Vectors</topic><topic>Vectors (Biology)</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Woodruff, Elise</creatorcontrib><creatorcontrib>Hardy, Nate B.</creatorcontrib><collection>Open Access: Wiley-Blackwell Open Access Journals</collection><collection>Wiley Free Archive</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Ecology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Woodruff, Elise</au><au>Hardy, Nate B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Virulence Evolution via Pleiotropy in Vector‐Borne Plant Pathogens</atitle><jtitle>Ecology and evolution</jtitle><addtitle>Ecol Evol</addtitle><date>2024-12</date><risdate>2024</risdate><volume>14</volume><issue>12</issue><spage>e70741</spage><epage>n/a</epage><pages>e70741-n/a</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>ABSTRACT
The dynamics of virulence evolution in vector‐borne plant pathogens can be complex. Here, we use individual‐based, quantitative‐genetic simulations to investigate how virulence evolution depends on genetic trade‐offs and population structure. Although quite generic, the model is inspired by the ecology of the plant‐pathogenic bacterium Xylella fastidiosa, and we use it to gain insights into possible modes of virulence evolution in that group. In particular, we aim to sharpen our intuition about how virulence may evolve over short time scales via antagonistically pleiotropic alleles affecting pathogen performance within hosts and vectors. We find that even when pathogens find themselves much more often in hosts than vectors, selection in the vector environment can cause correlational and potentially non‐adaptive changes in virulence in the host. The extent of such correlational virulence evolution depends on many system parameters, including the pathogen transmission rate, the proportion of the pathogen population occurring in hosts, the strengths of selection in host and vector environments, and the functional relationship between pathogen load and virulence. But there is a statistical interaction between the strength of selection in vectors and the proportion of the pathogen population in hosts, such that if within‐vector selection is strong enough, over the short term, it can dominate virulence evolution, even when the host environment predominates.
In general, natural selection is more efficient in more commonly encountered habitats. Here, with evolutionary simulations, we show that even when vector‐borne pathogens much more often occur within hosts, correlational and potentially maladaptive virulence evolution can be driven by selection in vectors.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>39687580</pmid><doi>10.1002/ece3.70741</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-6133-7086</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptive systems Agroecology Applied Ecology Disease Ecology Disease transmission Dynamic structural analysis Equilibrium Evolution Evolution & development Evolutionary Ecology Genomes Genotype & phenotype Habitats Microbial Ecology Mortality Mutation Normal distribution Parasitology Pathogens Pleiotropy Population (statistical) Population Genetics Population structure Quantitative Genetics Simulation Vectors Vectors (Biology) Virulence |
title | Virulence Evolution via Pleiotropy in Vector‐Borne Plant Pathogens |
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