Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns

To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between...

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Tipo de recurso:
Fecha de publicación:
2019
Institución:
Universidad del Rosario
Repositorio:
Repositorio EdocUR - U. Rosario
Idioma:
eng
OAI Identifier:
oai:repository.urosario.edu.co:10336/23799
Acceso en línea:
https://doi.org/10.1016/j.cub.2019.10.010
https://repository.urosario.edu.co/handle/10336/23799
Palabra clave:
Article
Butterfly
Convergent evolution
Crispr-cas9 system
Knockout gene
Mullerian mimicry
Natural selection
Nonhuman
Site directed mutagenesis
Wing
Wnt signaling
Butterfly wing patterns
Color patterns
Convergent evolution
Crispr mutagenesis
Heliconius butterflies
Müllerian mimicry
Wnt signaling
Wnta
Rights
License
Abierto (Texto Completo)
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network_acronym_str EDOCUR2
network_name_str Repositorio EdocUR - U. Rosario
repository_id_str
dc.title.spa.fl_str_mv Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
title Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
spellingShingle Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
Article
Butterfly
Convergent evolution
Crispr-cas9 system
Knockout gene
Mullerian mimicry
Natural selection
Nonhuman
Site directed mutagenesis
Wing
Wnt signaling
Butterfly wing patterns
Color patterns
Convergent evolution
Crispr mutagenesis
Heliconius butterflies
Müllerian mimicry
Wnt signaling
Wnta
title_short Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
title_full Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
title_fullStr Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
title_full_unstemmed Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
title_sort Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
dc.subject.keyword.spa.fl_str_mv Article
Butterfly
Convergent evolution
Crispr-cas9 system
Knockout gene
Mullerian mimicry
Natural selection
Nonhuman
Site directed mutagenesis
Wing
Wnt signaling
Butterfly wing patterns
Color patterns
Convergent evolution
Crispr mutagenesis
Heliconius butterflies
Müllerian mimicry
Wnt signaling
Wnta
topic Article
Butterfly
Convergent evolution
Crispr-cas9 system
Knockout gene
Mullerian mimicry
Natural selection
Nonhuman
Site directed mutagenesis
Wing
Wnt signaling
Butterfly wing patterns
Color patterns
Convergent evolution
Crispr mutagenesis
Heliconius butterflies
Müllerian mimicry
Wnt signaling
Wnta
description To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5–4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three co-mimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the co-mimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation. © 2019 Elsevier LtdConcha et al. use CRISPR/Cas9 genome editing to knock out a major wing patterning gene, WntA, in mimetic species of Heliconius butterflies and report that WntA is used in divergent gene regulatory networks in co-mimics and that resemblance is achieved through differential expression of WntA and its interaction with the specific genetic background. © 2019 Elsevier Ltd
publishDate 2019
dc.date.created.spa.fl_str_mv 2019
dc.date.accessioned.none.fl_str_mv 2020-05-26T00:05:29Z
dc.date.available.none.fl_str_mv 2020-05-26T00:05:29Z
dc.type.eng.fl_str_mv article
dc.type.coarversion.fl_str_mv http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_6501
dc.type.spa.spa.fl_str_mv Artículo
dc.identifier.doi.none.fl_str_mv https://doi.org/10.1016/j.cub.2019.10.010
dc.identifier.issn.none.fl_str_mv 9609822
dc.identifier.uri.none.fl_str_mv https://repository.urosario.edu.co/handle/10336/23799
url https://doi.org/10.1016/j.cub.2019.10.010
https://repository.urosario.edu.co/handle/10336/23799
identifier_str_mv 9609822
dc.language.iso.spa.fl_str_mv eng
language eng
dc.relation.citationEndPage.none.fl_str_mv 4009.e4
dc.relation.citationIssue.none.fl_str_mv No. 23
dc.relation.citationStartPage.none.fl_str_mv 3996
dc.relation.citationTitle.none.fl_str_mv Current Biology
dc.relation.citationVolume.none.fl_str_mv Vol. 29
dc.relation.ispartof.spa.fl_str_mv Current Biology, ISSN:9609822, Vol.29, No.23 (2019); pp. 3996-4009.e4
dc.relation.uri.spa.fl_str_mv https://www.scopus.com/inward/record.uri?eid=2-s2.0-85075449549&doi=10.1016%2fj.cub.2019.10.010&partnerID=40&md5=7a669358537527a3745bcf5c9be5b829
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.rights.acceso.spa.fl_str_mv Abierto (Texto Completo)
rights_invalid_str_mv Abierto (Texto Completo)
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dc.format.mimetype.none.fl_str_mv application/pdf
dc.publisher.spa.fl_str_mv Cell Press
institution Universidad del Rosario
dc.source.instname.spa.fl_str_mv instname:Universidad del Rosario
dc.source.reponame.spa.fl_str_mv reponame:Repositorio Institucional EdocUR
repository.name.fl_str_mv Repositorio institucional EdocUR
repository.mail.fl_str_mv edocur@urosario.edu.co
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spelling 40268c7c-d844-4b92-bd4e-85500756f61ed31dbea4-791a-4fd5-aa47-4db8d1849fb960f72356-364c-41f0-961e-cbfa4ef5c553dadcc730-ab50-4a48-8f36-6bb0c83350d0f56f53cd-9cc5-4ae7-9f4a-09cabacfd4b9be002f1c-92bd-4a7b-8359-43085ef421ce3dcac7e4-191b-4389-9a22-3db38a22de81d07fe46f-5ffb-48c7-9dcc-f801cd93f05824dcd470-f3f7-42b5-a0c7-c21558d751860bc78994-1002-41d0-b2f7-24421554c738ef968940-143d-4599-b9eb-df0a1a59e3fb506f9ba5-db29-45a0-a3a7-0067e637cc1e633643e8-2064-43f4-b9ca-a08a7c8619f296364e9e-d17b-4cf5-87f2-b26459a295f9ab30925b-1b0c-472d-94be-6f5efad8506a531073116007987375760079142324600219c41fc-a7b2-4482-86a3-19e7976fff600b8864d7-f67f-4c82-b343-c58c95b93b24da27e778-e603-42f2-b966-60efe8d6609dcbc4cc4c-8ac4-476a-9dd6-26a30b49fffbd207a325-5c4e-44b5-a7aa-9624a8ebbc97eab3e865-70a3-45f8-8314-06769c9d9ac987ee514d-dccc-40c5-bc92-6375cde000e42020-05-26T00:05:29Z2020-05-26T00:05:29Z2019To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5–4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three co-mimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the co-mimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation. © 2019 Elsevier LtdConcha et al. use CRISPR/Cas9 genome editing to knock out a major wing patterning gene, WntA, in mimetic species of Heliconius butterflies and report that WntA is used in divergent gene regulatory networks in co-mimics and that resemblance is achieved through differential expression of WntA and its interaction with the specific genetic background. © 2019 Elsevier Ltdapplication/pdfhttps://doi.org/10.1016/j.cub.2019.10.0109609822https://repository.urosario.edu.co/handle/10336/23799engCell Press4009.e4No. 233996Current BiologyVol. 29Current Biology, ISSN:9609822, Vol.29, No.23 (2019); pp. 3996-4009.e4https://www.scopus.com/inward/record.uri?eid=2-s2.0-85075449549&doi=10.1016%2fj.cub.2019.10.010&partnerID=40&md5=7a669358537527a3745bcf5c9be5b829Abierto (Texto Completo)http://purl.org/coar/access_right/c_abf2instname:Universidad del Rosarioreponame:Repositorio Institucional EdocURArticleButterflyConvergent evolutionCrispr-cas9 systemKnockout geneMullerian mimicryNatural selectionNonhumanSite directed mutagenesisWingWnt signalingButterfly wing patternsColor patternsConvergent evolutionCrispr mutagenesisHeliconius butterfliesMüllerian mimicryWnt signalingWntaInterplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing PatternsarticleArtículohttp://purl.org/coar/version/c_970fb48d4fbd8a85http://purl.org/coar/resource_type/c_6501Concha C.Wallbank R.W.R.Hanly J.J.Fenner J.Livraghi L.Rivera E.S.Paulo D.F.Arias C.Vargas M.Sanjeev M.Morrison C.Tian D.Aguirre P.Ferrara S.Foley J.Pardo Díaz, Geimy CarolinaSalazar, CamiloLinares, MauricioMassardo D.Counterman B.A.Scott M.J.Jiggins C.D.Papa R.Martin A.McMillan W.O.10336/23799oai:repository.urosario.edu.co:10336/237992022-05-02 07:37:17.262169https://repository.urosario.edu.coRepositorio institucional EdocURedocur@urosario.edu.co