Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism
A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations...
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Veröffentlicht in: | The American naturalist 2015-06, Vol.185 (6), p.E182-E196 |
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description | A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood–based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available. |
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One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood–based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available.</description><identifier>ISSN: 0003-0147</identifier><identifier>EISSN: 1537-5323</identifier><identifier>DOI: 10.1086/680982</identifier><identifier>PMID: 25996869</identifier><identifier>CODEN: AMNTA4</identifier><language>eng</language><publisher>United States: University of Chicago Press</publisher><subject>Alleles ; Animal reproduction ; Animals ; balancing ; Biologi ; Biological Evolution ; Biological Sciences ; color polymorphism ; E-Article ; Ecological balance ; Ecological genetics ; Evolutionary Biology ; Evolutionary genetics ; Evolutionsbiologi ; Female ; Female animals ; Genetic diversity ; Genetic Variation ; Genetics, Population ; Insects ; Ischnura elegans ; Likelihood Functions ; Male ; Mating behavior ; Mating Preference, Animal ; maximum likelihood ; Modeling ; Models, Genetic ; Natural Sciences ; Naturvetenskap ; negative frequency-dependent selection ; Odonata - genetics ; Parametric models ; Pigmentation ; Polymorphism ; Polymorphism, Genetic ; Population genetics ; selection ; Time series</subject><ispartof>The American naturalist, 2015-06, Vol.185 (6), p.E182-E196</ispartof><rights>2015 by The University of Chicago. All rights reserved.</rights><rights>Copyright University of Chicago, acting through its Press Jun 2015</rights><rights>info:eu-repo/semantics/openAccess</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c621t-b83e01ebdf50cfbbcc28ca7f864b633154ac602950f4803666aba71f2f6f261f3</citedby><cites>FETCH-LOGICAL-c621t-b83e01ebdf50cfbbcc28ca7f864b633154ac602950f4803666aba71f2f6f261f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,799,881,26544,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25996869$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://lup.lub.lu.se/record/7410583$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Troy Day</contributor><contributor>Vlastimil Křivan</contributor><creatorcontrib>Le Rouzic, Arnaud</creatorcontrib><creatorcontrib>Hansen, Thomas F.</creatorcontrib><creatorcontrib>Gosden, Thomas P.</creatorcontrib><creatorcontrib>Svensson, Erik I.</creatorcontrib><title>Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism</title><title>The American naturalist</title><addtitle>Am Nat</addtitle><description>A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood–based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available.</description><subject>Alleles</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>balancing</subject><subject>Biologi</subject><subject>Biological Evolution</subject><subject>Biological Sciences</subject><subject>color polymorphism</subject><subject>E-Article</subject><subject>Ecological balance</subject><subject>Ecological genetics</subject><subject>Evolutionary Biology</subject><subject>Evolutionary genetics</subject><subject>Evolutionsbiologi</subject><subject>Female</subject><subject>Female animals</subject><subject>Genetic diversity</subject><subject>Genetic Variation</subject><subject>Genetics, Population</subject><subject>Insects</subject><subject>Ischnura elegans</subject><subject>Likelihood Functions</subject><subject>Male</subject><subject>Mating behavior</subject><subject>Mating Preference, Animal</subject><subject>maximum likelihood</subject><subject>Modeling</subject><subject>Models, Genetic</subject><subject>Natural Sciences</subject><subject>Naturvetenskap</subject><subject>negative frequency-dependent selection</subject><subject>Odonata - genetics</subject><subject>Parametric models</subject><subject>Pigmentation</subject><subject>Polymorphism</subject><subject>Polymorphism, Genetic</subject><subject>Population genetics</subject><subject>selection</subject><subject>Time series</subject><issn>0003-0147</issn><issn>1537-5323</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>3HK</sourceid><recordid>eNqNkl-L1DAUxYso7rrqR9CAIr5U86dJk8dl3VFhRHHW55CktzMZ2qYm7ep8ezPO7g4IopBLCPxycs69KYqnBL8hWIq3QmIl6b3ilHBWl5xRdr84xRizEpOqPikepbTNR1Up_rA4oVwpIYU6LX5eXodunnwYTNyhK99DuYLoIaHzwXS75BP6CtdguoSmDaCVXw9mmiOg0KJFhO8zDG5XvoMRhgaGCa2gA7eXQ3kZtIDedIA-mckPa_QldLs-xHHjU_-4eNBmVXhys58V3xaXVxcfyuXn9x8vzpelE5RMpZUMMAHbtBy71lrnqHSmbqWorGCM8Mo4ganiuK0kZkIIY01NWtqKlgrSsrNiedBNP2CcrR6j73NUHYzX3Tzmsrl0Ao2ZhXyTayMbqisilJaKKV1V1jSNxA04k-WeH-Rc9CmH0kOIRucRcKp5jaXMxOsDMcaQ25Mm3fvkoOvMAGFOmtSYcJy91f9GhaRS1ozzjL74A92GOeYR_aa4opWo9tSrW3chpQjtXVyC9yaFPvyTDD67kZttD80ddvsxjtZmt_HOrMMYIaXjowcdPTb7Dr_8D_SYYJumEP9m7Bey59w9</recordid><startdate>20150601</startdate><enddate>20150601</enddate><creator>Le Rouzic, Arnaud</creator><creator>Hansen, Thomas F.</creator><creator>Gosden, Thomas P.</creator><creator>Svensson, Erik I.</creator><general>University of Chicago Press</general><general>University of Chicago, acting through its Press</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>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>3HK</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D95</scope></search><sort><creationdate>20150601</creationdate><title>Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism</title><author>Le Rouzic, Arnaud ; Hansen, Thomas F. ; Gosden, Thomas P. ; Svensson, Erik I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c621t-b83e01ebdf50cfbbcc28ca7f864b633154ac602950f4803666aba71f2f6f261f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Alleles</topic><topic>Animal reproduction</topic><topic>Animals</topic><topic>balancing</topic><topic>Biologi</topic><topic>Biological Evolution</topic><topic>Biological Sciences</topic><topic>color polymorphism</topic><topic>E-Article</topic><topic>Ecological balance</topic><topic>Ecological genetics</topic><topic>Evolutionary Biology</topic><topic>Evolutionary genetics</topic><topic>Evolutionsbiologi</topic><topic>Female</topic><topic>Female animals</topic><topic>Genetic diversity</topic><topic>Genetic Variation</topic><topic>Genetics, Population</topic><topic>Insects</topic><topic>Ischnura elegans</topic><topic>Likelihood Functions</topic><topic>Male</topic><topic>Mating behavior</topic><topic>Mating Preference, Animal</topic><topic>maximum likelihood</topic><topic>Modeling</topic><topic>Models, Genetic</topic><topic>Natural Sciences</topic><topic>Naturvetenskap</topic><topic>negative frequency-dependent selection</topic><topic>Odonata - genetics</topic><topic>Parametric models</topic><topic>Pigmentation</topic><topic>Polymorphism</topic><topic>Polymorphism, Genetic</topic><topic>Population genetics</topic><topic>selection</topic><topic>Time series</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Le Rouzic, Arnaud</creatorcontrib><creatorcontrib>Hansen, Thomas F.</creatorcontrib><creatorcontrib>Gosden, Thomas P.</creatorcontrib><creatorcontrib>Svensson, Erik 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>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>NORA - Norwegian Open Research Archives</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Lunds universitet</collection><jtitle>The American naturalist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Le Rouzic, Arnaud</au><au>Hansen, Thomas F.</au><au>Gosden, Thomas P.</au><au>Svensson, Erik I.</au><au>Troy Day</au><au>Vlastimil Křivan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism</atitle><jtitle>The American naturalist</jtitle><addtitle>Am Nat</addtitle><date>2015-06-01</date><risdate>2015</risdate><volume>185</volume><issue>6</issue><spage>E182</spage><epage>E196</epage><pages>E182-E196</pages><issn>0003-0147</issn><eissn>1537-5323</eissn><coden>AMNTA4</coden><abstract>A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood–based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available.</abstract><cop>United States</cop><pub>University of Chicago Press</pub><pmid>25996869</pmid><doi>10.1086/680982</doi><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Animal reproduction Animals balancing Biologi Biological Evolution Biological Sciences color polymorphism E-Article Ecological balance Ecological genetics Evolutionary Biology Evolutionary genetics Evolutionsbiologi Female Female animals Genetic diversity Genetic Variation Genetics, Population Insects Ischnura elegans Likelihood Functions Male Mating behavior Mating Preference, Animal maximum likelihood Modeling Models, Genetic Natural Sciences Naturvetenskap negative frequency-dependent selection Odonata - genetics Parametric models Pigmentation Polymorphism Polymorphism, Genetic Population genetics selection Time series |
title | Evolutionary Time-Series Analysis Reveals the Signature of Frequency-Dependent Selection on a Female Mating Polymorphism |
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