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

Rémi Allio (), Benoit Nabholz, Stefan Wanke, Guillaume Chomicki, Oscar A. Pérez-Escobar, Adam M. Cotton, Anne-Laure Clamens, Gaël J. Kergoat, Felix A. H. Sperling and Fabien L. Condamine ()
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Rémi Allio: Université de Montpellier
Benoit Nabholz: Université de Montpellier
Stefan Wanke: Technische Universität Dresden
Guillaume Chomicki: Durham University
Oscar A. Pérez-Escobar: Royal Botanic Gardens
Adam M. Cotton: Tambon Nong Kwai
Anne-Laure Clamens: Univ. Montpellier
Gaël J. Kergoat: Univ. Montpellier
Felix A. H. Sperling: University of Alberta
Fabien L. Condamine: Université de Montpellier

Nature Communications, 2021, vol. 12, issue 1, 1-15

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-020-20507-3

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