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

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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.

Edité par CCSD ; Nature Publishing Group -

International audience. 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.

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