Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution o...

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Autores: Orteu, Anna, Kucka, Marek, Gordon, Iain J., Ng’iru, Ivy, van der Heijden, Eva S. M., Talavera, Gerard, Warren, Ian A., Collins, Steve, ffrench-Constant, Richard H., Martins, Dino J., Frank Chan, Yingguang, Jiggins, Chris D., Martin, Simon H.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/352409
Acceso en línea:http://hdl.handle.net/10261/352409
Access Level:acceso abierto
Palabra clave:Transposable elements
Mimicry
Adaptive evolution
Linked-reads
Bioinformatic methods
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spelling Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippusOrteu, AnnaKucka, MarekGordon, Iain J.Ng’iru, Ivyvan der Heijden, Eva S. M.Talavera, GerardWarren, Ian A.Collins, Steveffrench-Constant, Richard H.Martins, Dino J.Frank Chan, YingguangJiggins, Chris D.Martin, Simon H.Transposable elementsMimicryAdaptive evolutionLinked-readsBioinformatic methodsHypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved an ancestral wing pattern present in other Hypolimnas species, repurposing it for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, and our new analytical tool, Wrath, we discover two large transposable element insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that, in the derived allele, the transposable elements disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.This work was supported by the Natural Environment Research Council (grant number NE/L002507/1 to A.O.); the Varley-Gradwell Travelling Fellowship in Insect Ecology 2021 from the University of Oxford to A.O.; the Student Research Award from the American Society of Naturalists to A.O., and the Lepidopterists’ Society Ron Leuschner Memorial Fund for Research from the Lepidopterists' Society. S.H.M. was supported by a University Research Fellowship from the Royal Society (grant number URF\R1\180682).Abstract Introduction Results Wrath: A Tool for Visualizing and Detecting Candidate SVs From Linked-Read Data Wrath Identifies SVs From Simulated Data, But Is Limited by Molecule Size and Window Size Multiple Deletions Are Found at the Optix Color Locus H. melpomene and H. erato Forewing Mimicry in H. misippus Is Controlled by the M Locus misippus Individuals Carry Multiple TE Insertions at the M Locus The M Allele Carrying TE Insertions Is Derived and Produces an Atavistic Adaptive Phenotype Discussion Methods Supplementary Material Acknowledgments Author Contributions Funding Data Availability References Supplementary dataOxford University PressNatural Environment Research Council (UK)University of OxfordAmerican Society of NaturalistsLepidopterists' SocietyRoyal Society (UK)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2024202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/352409reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://dx.doi.org/10.1093/molbev/msae041Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3524092026-05-22T06:33:51Z
dc.title.none.fl_str_mv Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
title Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
spellingShingle Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
Orteu, Anna
Transposable elements
Mimicry
Adaptive evolution
Linked-reads
Bioinformatic methods
title_short Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
title_full Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
title_fullStr Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
title_full_unstemmed Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
title_sort Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus
dc.creator.none.fl_str_mv Orteu, Anna
Kucka, Marek
Gordon, Iain J.
Ng’iru, Ivy
van der Heijden, Eva S. M.
Talavera, Gerard
Warren, Ian A.
Collins, Steve
ffrench-Constant, Richard H.
Martins, Dino J.
Frank Chan, Yingguang
Jiggins, Chris D.
Martin, Simon H.
author Orteu, Anna
author_facet Orteu, Anna
Kucka, Marek
Gordon, Iain J.
Ng’iru, Ivy
van der Heijden, Eva S. M.
Talavera, Gerard
Warren, Ian A.
Collins, Steve
ffrench-Constant, Richard H.
Martins, Dino J.
Frank Chan, Yingguang
Jiggins, Chris D.
Martin, Simon H.
author_role author
author2 Kucka, Marek
Gordon, Iain J.
Ng’iru, Ivy
van der Heijden, Eva S. M.
Talavera, Gerard
Warren, Ian A.
Collins, Steve
ffrench-Constant, Richard H.
Martins, Dino J.
Frank Chan, Yingguang
Jiggins, Chris D.
Martin, Simon H.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Natural Environment Research Council (UK)
University of Oxford
American Society of Naturalists
Lepidopterists' Society
Royal Society (UK)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Transposable elements
Mimicry
Adaptive evolution
Linked-reads
Bioinformatic methods
topic Transposable elements
Mimicry
Adaptive evolution
Linked-reads
Bioinformatic methods
description Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved an ancestral wing pattern present in other Hypolimnas species, repurposing it for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, and our new analytical tool, Wrath, we discover two large transposable element insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that, in the derived allele, the transposable elements disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/352409
url http://hdl.handle.net/10261/352409
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv http://dx.doi.org/10.1093/molbev/msae041
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812429

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