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

Author:

Allio RémiORCID,Nabholz BenoitORCID,Wanke Stefan,Chomicki GuillaumeORCID,Pérez-Escobar Oscar A.ORCID,Cotton Adam M.ORCID,Clamens Anne-Laure,Kergoat Gaël J.ORCID,Sperling Felix A.H.ORCID,Condamine Fabien L.ORCID

Abstract

The exuberant proliferation of herbivorous insects is attributed to their 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 unique 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.

Publisher

Cold Spring Harbor Laboratory

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