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

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.

The evolution of coevolution in the study of species interactions

“…2006, Fordyce 2010, Allio et al. 2021). For a specialist herbivore, host shifts can happen through 1) switching directly from one host to the next, or 2) an intermediate stage of host range expansion followed by subsequent specialization.…”

To pest, or not to pest: comparative transcriptomics and genomics towards an understanding of polyphagous pest Noctuidae

“…The success and evolution of Lepidoptera is closely linked to their relation with plants. The coevolutionary interactions between plants and Lepidoptera, with evolving plant defences and counter adaptations by the herbivore, has resulted in gene and genome dynamics that fuel adaptations and diversification rates (Allio et al, 2021;Edger et al, 2015;Gloss et al, 2019;Simon, d'Alencon, Guy, Jacquin-Joly, Jaquiery, et al, 2015). Indeed, the origin of plant defences and evolved counterresponses are associated with shifts in diversification rates in Lepidoptera (Edger et al, 2015).…”

“…Indeed, the origin of plant defences and evolved counterresponses are associated with shifts in diversification rates in Lepidoptera (Edger et al, 2015). Furthermore, the dynamics of plant use in terms of host colonisations and host shifts have played profound roles in accelerated diversification rates in Lepidoptera (Allio et al, 2021;Fordyce, 2010;Menken et al, 2010;Nylin et al, 2018).…”

“…Furthermore, Lepidoptera are one of the largest radiations of plant-feeding insects, with plant feeding having evolved from inner plant tissue (via concealed external feeding) to exposed folivory (Menken et al, 2010;Mitter et al, 2017). The diversity of Lepidoptera and the expansion of the order have been linked to the close association with-and rise of angiosperms (Allio et al, 2021;Ehrlich & Raven, 1964;Mitter et al, 2017). The coevolutionary relationship through a process termed "escape-and-radiate" has long been hypothesised to be the driving force for the diversification of both flowering plants and butterflies (Ehrlich & Raven, 1964;Thompson, 1989).…”

“…The implementation of genome data has put studies focusing on the genetic basis of host plant use and host shifts into a new perspective (Allio et al, 2021;Nallu et al, 2018). For example, the genomes of polyphagous species are often associated with expansions in gene families involved in plant feeding, such as chemoreception and detoxification (Calla et al, 2017;Xu et al, 2016).…”