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Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants

Allio, Rémi; Nabholz, Benoit; Wanke, Stefan; Chomicki, Guillaume; Pérez-Escobar, Oscar A.; Cotton, Adam M.; Clamens, Anne-Laure; Kergoat, Gaël J.; Sperling, Felix A.H.; Condamine, Fabien L.

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Authors

Rémi Allio

Benoit Nabholz

Stefan Wanke

Oscar A. Pérez-Escobar

Adam M. Cotton

Anne-Laure Clamens

Gaël J. Kergoat

Felix A.H. Sperling

Fabien L. Condamine



Abstract

The mega-diversity of herbivorous insects is attributed to their co-evolutionary associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a valuable opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide adaptations and macroevolutionary consequences, lending support to the importance of ecological interactions as evolutionary drivers over long time periods.

Citation

Allio, R., Nabholz, B., Wanke, S., Chomicki, G., Pérez-Escobar, O. A., Cotton, A. M., …Condamine, F. L. (2021). Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants. Nature Communications, 12, Article 354. https://doi.org/10.1038/s41467-020-20507-3

Journal Article Type Article
Acceptance Date Dec 3, 2020
Online Publication Date Jan 13, 2021
Publication Date 2021
Deposit Date Jun 4, 2021
Publicly Available Date Jun 4, 2021
Journal Nature Communications
Publisher Nature Research
Peer Reviewed Peer Reviewed
Volume 12
Article Number 354
DOI https://doi.org/10.1038/s41467-020-20507-3
Public URL https://durham-repository.worktribe.com/output/1247385

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http://creativecommons.org/licenses/by/4.0/

Copyright Statement
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.





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