Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato
Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius sp...
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Published in | PloS one Vol. 8; no. 3; p. e57033 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
22.03.2013
Public Library of Science (PLoS) |
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Abstract | Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato, we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis, to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato. We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change. |
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AbstractList | Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato, we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis, to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato. We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change. Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato , we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis , to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato . We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change. |
Audience | Academic |
Author | McMillan, W Owen Reed, Robert D Nijhout, H Frederik Maldonado, Karla Lindstrom, Daniel P Papa, Riccardo Hrbek, Tomas Kapan, Durrell D Counterman, Brian A |
AuthorAffiliation | 5 Department of Biology, University of Guam, Mangilao, Guam 3 Center for Conservation and Research Training, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America Oxford Brookes University, United Kingdom 2 Department of Entomology and Center for Comparative Genomics, California Academy of Sciences, San Francisco, California, United States of America 4 Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi, United States of America 6 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, United States of America 1 Department of Biology and Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico 7 Department of Biology, Duke University, Durham, North Carolina, United States of America 8 Biology Department, Institute of Biological Sciences, Federal University of Amazonas, Manaus, AM, Brazil 9 Smithsonian Tropical Researc |
AuthorAffiliation_xml | – name: Oxford Brookes University, United Kingdom – name: 1 Department of Biology and Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico – name: 5 Department of Biology, University of Guam, Mangilao, Guam – name: 8 Biology Department, Institute of Biological Sciences, Federal University of Amazonas, Manaus, AM, Brazil – name: 6 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, United States of America – name: 7 Department of Biology, Duke University, Durham, North Carolina, United States of America – name: 3 Center for Conservation and Research Training, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America – name: 2 Department of Entomology and Center for Comparative Genomics, California Academy of Sciences, San Francisco, California, United States of America – name: 4 Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi, United States of America – name: 9 Smithsonian Tropical Research Institute, Panama City, Panama |
Author_xml | – sequence: 1 givenname: Riccardo surname: Papa fullname: Papa, Riccardo email: rpapa.lab@gmail.com organization: Department of Biology and Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico. rpapa.lab@gmail.com – sequence: 2 givenname: Durrell D surname: Kapan fullname: Kapan, Durrell D – sequence: 3 givenname: Brian A surname: Counterman fullname: Counterman, Brian A – sequence: 4 givenname: Karla surname: Maldonado fullname: Maldonado, Karla – sequence: 5 givenname: Daniel P surname: Lindstrom fullname: Lindstrom, Daniel P – sequence: 6 givenname: Robert D surname: Reed fullname: Reed, Robert D – sequence: 7 givenname: H Frederik surname: Nijhout fullname: Nijhout, H Frederik – sequence: 8 givenname: Tomas surname: Hrbek fullname: Hrbek, Tomas – sequence: 9 givenname: W Owen surname: McMillan fullname: McMillan, W Owen |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23533571$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2013 Public Library of Science 2013 Papa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Papa et al 2013 Papa et al |
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DocumentTitleAlternate | Genetic Control of Wing Color Pattern in H. erato |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Provided fundamental edits to the manuscript: DDK RDR HFN WOM. Conceived and designed the experiments: DDK WOM. Performed the experiments: RP DDK KM WOM. Analyzed the data: RP TH. Contributed reagents/materials/analysis tools: BAC DPL RDR HFN. Wrote the paper: RP. |
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Turner |
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Snippet | Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work... Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work... |
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SubjectTerms | Adaptive control Agriculture Alleles Amplified fragment length polymorphism Analysis Animals Biology Butterflies Butterflies & moths Butterflies - genetics Butterflies - metabolism Chromosome Mapping Color Ecology Empirical analysis Evolution Evolution & development Gene mapping Genes Genetic analysis Genetic crosses Genetic research Genomics Homology Insect Proteins - genetics Insect Proteins - metabolism Loci Offspring Pigmentation - genetics Pigmentation - physiology Quantitative genetics Quantitative Trait Loci Radiation Science Variation Wings, Animal - metabolism |
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Title | Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato |
URI | https://www.ncbi.nlm.nih.gov/pubmed/23533571 https://www.proquest.com/docview/1330893509/abstract/ https://search.proquest.com/docview/1321336894 https://pubmed.ncbi.nlm.nih.gov/PMC3606360 https://doaj.org/article/998cb9ec1c874bafb00efa87fd94d451 http://dx.doi.org/10.1371/journal.pone.0057033 |
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