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Inbreeding shapes the evolution of marine invertebrates
Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incom...
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Published in: | Evolution 2020-05, Vol.74 (5), p.871-882 |
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creator | Olsen, Kevin C. Ryan, Will H. Winn, Alice A. Kosman, Ellen T. Moscoso, Jose A. Krueger-Hadfield, Stacy A. Burgess, Scott C. Carlon, David B. Grosberg, Richard K. Kalisz, Susan Levitan, Don R. |
description | Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F
IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to selffertiliz, disperse, and choose mates. The similarity of F
IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F
IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization. |
doi_str_mv | 10.1111/evo.13951 |
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IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to selffertiliz, disperse, and choose mates. The similarity of F
IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F
IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.</description><identifier>ISSN: 0014-3820</identifier><identifier>EISSN: 1558-5646</identifier><identifier>DOI: 10.1111/evo.13951</identifier><identifier>PMID: 32191349</identifier><language>eng</language><publisher>United States: Wiley</publisher><subject>Algae ; Animal Distribution ; Animals ; Aquatic Organisms - genetics ; Aquatic Organisms - physiology ; Biological Evolution ; Breeding ; Evolution ; Fertilization ; Force distribution ; Gametes ; Genetic diversity ; Hermaphroditism ; Inbreeding ; Inbreeding depression ; Invertebrates ; Invertebrates - genetics ; Invertebrates - physiology ; Life cycles ; Life history ; Life History Traits ; marine invertebrate ; Marine invertebrates ; Marine organisms ; mating system ; Modular construction ; Natural selection ; Original ; ORIGINAL ARTICLE ; Outbreeding ; Plant breeding ; Plant Dispersal ; Purging ; Seaweed - genetics ; Seaweed - physiology ; Seaweeds ; Self-fertilization ; Stress concentration ; Tracheophyta - genetics ; Tracheophyta - physiology</subject><ispartof>Evolution, 2020-05, Vol.74 (5), p.871-882</ispartof><rights>2020 The Authors</rights><rights>2020 The Authors. published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.</rights><rights>2020 The Authors. Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.</rights><rights>2020. This article 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><rights>2020 The Authors. published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4651-a6547462c5f49897302c52e01a2f1361f14ec5212d7a6bc4d9509bb61bf08e8a3</citedby><cites>FETCH-LOGICAL-c4651-a6547462c5f49897302c52e01a2f1361f14ec5212d7a6bc4d9509bb61bf08e8a3</cites><orcidid>0000-0001-5318-3312 ; 0000-0002-0348-3453 ; 0000-0002-7324-7448</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/48577557$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/48577557$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32191349$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Olsen, Kevin C.</creatorcontrib><creatorcontrib>Ryan, Will H.</creatorcontrib><creatorcontrib>Winn, Alice A.</creatorcontrib><creatorcontrib>Kosman, Ellen T.</creatorcontrib><creatorcontrib>Moscoso, Jose A.</creatorcontrib><creatorcontrib>Krueger-Hadfield, Stacy A.</creatorcontrib><creatorcontrib>Burgess, Scott C.</creatorcontrib><creatorcontrib>Carlon, David B.</creatorcontrib><creatorcontrib>Grosberg, Richard K.</creatorcontrib><creatorcontrib>Kalisz, Susan</creatorcontrib><creatorcontrib>Levitan, Don R.</creatorcontrib><title>Inbreeding shapes the evolution of marine invertebrates</title><title>Evolution</title><addtitle>Evolution</addtitle><description>Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F
IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to selffertiliz, disperse, and choose mates. The similarity of F
IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F
IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.</description><subject>Algae</subject><subject>Animal Distribution</subject><subject>Animals</subject><subject>Aquatic Organisms - genetics</subject><subject>Aquatic Organisms - physiology</subject><subject>Biological Evolution</subject><subject>Breeding</subject><subject>Evolution</subject><subject>Fertilization</subject><subject>Force distribution</subject><subject>Gametes</subject><subject>Genetic diversity</subject><subject>Hermaphroditism</subject><subject>Inbreeding</subject><subject>Inbreeding depression</subject><subject>Invertebrates</subject><subject>Invertebrates - genetics</subject><subject>Invertebrates - physiology</subject><subject>Life cycles</subject><subject>Life history</subject><subject>Life History Traits</subject><subject>marine invertebrate</subject><subject>Marine invertebrates</subject><subject>Marine organisms</subject><subject>mating system</subject><subject>Modular construction</subject><subject>Natural selection</subject><subject>Original</subject><subject>ORIGINAL ARTICLE</subject><subject>Outbreeding</subject><subject>Plant breeding</subject><subject>Plant Dispersal</subject><subject>Purging</subject><subject>Seaweed - genetics</subject><subject>Seaweed - physiology</subject><subject>Seaweeds</subject><subject>Self-fertilization</subject><subject>Stress concentration</subject><subject>Tracheophyta - genetics</subject><subject>Tracheophyta - physiology</subject><issn>0014-3820</issn><issn>1558-5646</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kc9LHDEUx0Np0VV76B_QMuBFD6N5-TFJLkIRawXBS-01ZGbfuFlmk20ys8X_3tjVxRaaS0LyeR9evo-QT0DPoKxz3MQz4EbCOzIDKXUtG9G8JzNKQdRcM7pPDnJeUkoLY_bIPmdggAszI-omtAlx7sNDlRdujbkaF1gV4zCNPoYq9tXKJR-w8mGDacQ2uRHzEfnQuyHjx5f9kNx_u_px-b2-vbu-ufx6W3eikVC7RgolGtbJXhhtFKflyJCCYz3wBnoQWC6AzZVr2k7MjaSmbRtoe6pRO35ILrbe9dSucN5hGJMb7Dr50tWjjc7bv1-CX9iHuLGKa64oFMHJiyDFXxPm0a587nAYXMA4Zcu4MpRxLXVBj_9Bl3FKoXzPMkGZeA6PFup0S3Up5pyw3zUD1D6Pw5bw7J9xFPbL2-535Gv-BTjfAr_9gI__N9mrn3evys_bimUeY9pVCC2VklLxJ7j3nR0</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Olsen, Kevin C.</creator><creator>Ryan, Will H.</creator><creator>Winn, Alice A.</creator><creator>Kosman, Ellen T.</creator><creator>Moscoso, Jose A.</creator><creator>Krueger-Hadfield, Stacy A.</creator><creator>Burgess, Scott C.</creator><creator>Carlon, David B.</creator><creator>Grosberg, Richard K.</creator><creator>Kalisz, Susan</creator><creator>Levitan, Don R.</creator><general>Wiley</general><general>Oxford University Press</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5318-3312</orcidid><orcidid>https://orcid.org/0000-0002-0348-3453</orcidid><orcidid>https://orcid.org/0000-0002-7324-7448</orcidid></search><sort><creationdate>202005</creationdate><title>Inbreeding shapes the evolution of marine invertebrates</title><author>Olsen, Kevin C. ; 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Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F
IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to selffertiliz, disperse, and choose mates. The similarity of F
IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F
IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.</abstract><cop>United States</cop><pub>Wiley</pub><pmid>32191349</pmid><doi>10.1111/evo.13951</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-5318-3312</orcidid><orcidid>https://orcid.org/0000-0002-0348-3453</orcidid><orcidid>https://orcid.org/0000-0002-7324-7448</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Algae Animal Distribution Animals Aquatic Organisms - genetics Aquatic Organisms - physiology Biological Evolution Breeding Evolution Fertilization Force distribution Gametes Genetic diversity Hermaphroditism Inbreeding Inbreeding depression Invertebrates Invertebrates - genetics Invertebrates - physiology Life cycles Life history Life History Traits marine invertebrate Marine invertebrates Marine organisms mating system Modular construction Natural selection Original ORIGINAL ARTICLE Outbreeding Plant breeding Plant Dispersal Purging Seaweed - genetics Seaweed - physiology Seaweeds Self-fertilization Stress concentration Tracheophyta - genetics Tracheophyta - physiology |
title | Inbreeding shapes the evolution of marine invertebrates |
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