Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)

Seasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid unsuitable conditions by migrating. Despite a growing understanding...

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Detalhes bibliográficos
Autores: Boman, Jesper, Zhu, Yishu, Höök, Lars, Vila, Roger, Talavera, Gerard, Backström, Niclas
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/332122
Acesso em linha:http://hdl.handle.net/10261/332122
https://doi.org/10.1111/mec.16957
Access Level:acceso abierto
Palavra-chave:DNA methylation
Environmental stress
Migration
Painted lady butterfly
Vanessa cardui
id ES_32022a35acf993c5c6afbcae669e3846
oai_identifier_str oai:digital.csic.es:10261/332122
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
title Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
spellingShingle Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
Boman, Jesper
DNA methylation
Environmental stress
Migration
Painted lady butterfly
Vanessa cardui
title_short Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
title_full Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
title_fullStr Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
title_full_unstemmed Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
title_sort Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
dc.creator.none.fl_str_mv Boman, Jesper
Zhu, Yishu
Höök, Lars
Vila, Roger
Talavera, Gerard
Backström, Niclas
author Boman, Jesper
author_facet Boman, Jesper
Zhu, Yishu
Höök, Lars
Vila, Roger
Talavera, Gerard
Backström, Niclas
author_role author
author2 Zhu, Yishu
Höök, Lars
Vila, Roger
Talavera, Gerard
Backström, Niclas
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Swedish Research Council for Sustainable Development
Knut and Alice Wallenberg Foundation
Science for Life Laboratory
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv DNA methylation
Environmental stress
Migration
Painted lady butterfly
Vanessa cardui
topic DNA methylation
Environmental stress
Migration
Painted lady butterfly
Vanessa cardui
description Seasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it remains unknown how individuals register and store environmental cues to determine whether and where to migrate. Here, we explored how competition and host plant availability during larval development affect patterns of DNA methylation in the migratory painted lady (Vanessa cardui) butterfly. We identify a set of potentially functional methylome shifts associated with differences in the environment, indicating that DNA methylation is involved in the response to different conditions during larval development. By analysing the transcriptome for the same samples used for methylation profiling, we also uncovered a non-monotonic relationship between gene body methylation and gene expression. Our results provide a starting point for understanding the interplay between DNA methylation and gene expression in butterflies in general and how differences in environmental conditions during development can trigger unique epigenetic marks that might be important for behavioural decisions in the adult stage.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
2023
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/10261/332122
https://doi.org/10.1111/mec.16957
url http://hdl.handle.net/10261/332122
https://doi.org/10.1111/mec.16957
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107078GB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-117739GA-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1111/mec.16957
https://doi.org/10.1111/mec.16957
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
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
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spelling Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)Boman, JesperZhu, YishuHöök, LarsVila, RogerTalavera, GerardBackström, NiclasDNA methylationEnvironmental stressMigrationPainted lady butterflyVanessa carduiSeasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it remains unknown how individuals register and store environmental cues to determine whether and where to migrate. Here, we explored how competition and host plant availability during larval development affect patterns of DNA methylation in the migratory painted lady (Vanessa cardui) butterfly. We identify a set of potentially functional methylome shifts associated with differences in the environment, indicating that DNA methylation is involved in the response to different conditions during larval development. By analysing the transcriptome for the same samples used for methylation profiling, we also uncovered a non-monotonic relationship between gene body methylation and gene expression. Our results provide a starting point for understanding the interplay between DNA methylation and gene expression in butterflies in general and how differences in environmental conditions during development can trigger unique epigenetic marks that might be important for behavioural decisions in the adult stage.This project was financially supported by a FORMAS research grant (2019-00670 to N.B.). The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. RNA sequencing was performed by the National Genomics Infrastructure in Genomics Production, Stockholm, funded by the Science for Life Laboratory, the Knut and Alice Wallenberg Foundation and the Swedish Research Council. We acknowledge the National Bioinformatics Infrastructure Sweden (NBIS) for granting WABI (Wallenberg Advanced Bioinformatics Infrastructure) support to the research group. R.V. was supported by the Spanish government through grant PID2019-107078GB-I00/MCIN/AEI/10.13039/501100011033. G.T. was supported by the project PID2020-117739GA-I00 MCIN/AEI/10.13039/501100011033. All authors were supported by the grant LINKA20399 from the CSIC iLINK programme.1 INTRODUCTION2 MATERIALS AND METHODSExperimental setupDNA extraction and bisulphite sequencingRNA extraction and sequencingProcessing of bisulphite sequence reads and methylation callingGene expression quantification and differential expression analysisMethylation levelGene profileDifferential methylation analysisGene ontology enrichment analysis and candidate gene identificationStatistical analysis3 RESULTSDNA methylation is concentrated in genic regionsMethylation levels along the gene body vary with gene expression levelsMost differentially methylated regions show higher methylation levels under stressFunctional analysis of genes enriched in differentially methylated regions between treatments reveals candidate pathways and genes involved in environmental responseDifferentially expressed genes are not enriched in differential methylation4 DISCUSSIONDiversification of methylation within Lepidoptera revealed by novel relationship with expressionStress during development shifts the methylation profile in adults but evidence for a relationship with differential expression remains elusiveDifferential methylation in an RNA methyltransferase gene: mettl3CaveatsOutlook5 CONCLUSIONAUTHOR CONTRIBUTIONSACKNOWLEDGEMENTSCONFLICT OF INTEREST STATEMENTJohn Wiley & SonsSwedish Research Council for Sustainable DevelopmentKnut and Alice Wallenberg FoundationScience for Life LaboratoryMinisterio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/332122https://doi.org/10.1111/mec.16957reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107078GB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-117739GA-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1111/mec.16957https://doi.org/10.1111/mec.16957Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3321222026-05-22T06:33:51Z
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