Myrmecophytism as a driver of macroevolutionary patterns: perspectives from the Southeast Asian Macaranga ant-plant symbiosis

Abstract

Myrmecophytes utilise defensive services offered by obligate ant partners in a novel means of survival in tropical habitats. Although much is known about the ecology of myrmecophytism, there arent enough empirical examples to demonstrate whether it substantially influences evolutionary patterns in host plant lineages. In this study, we make use of the species-rich Macaranga (Euphorbiaceae) ant-plant symbiosis distributed in Sundaland to delve into the evolutionary dynamics of myrmecophytism in host plants. We generated the most comprehensive dated phylogeny of myrmecophytic Macaranga till date using sequences derived from genotyping-by-sequencing (GBS), a next-generation sequencing (NGS) technique. With this in hand, we traced the evolutionary history of myrmecophytism in Macaranga using parametric biogeography and ancestral state reconstruction. Diversification rate analysis methods were employed to determine if myrmecophytism enhanced diversification rates in the genus. Our results demonstrate that myrmecophytism is plastic and easily lost unless it is overly specialised. Ancestral state reconstruction supported a single origin of myrmecophytism in Macaranga [~]18 mya on Borneo followed by multiple losses. Diversification rate analysis methods did not yield sufficient evidence to support the hypothesis that myrmecophytism enhanced diversification rates in Macaranga; we found that topographical features on Borneo may have played a more direct role in the divergence of clades instead. Through this comprehensive investigation of the evolution of myrmecophytism in Macaranga, our study also provides evidence that a key innovation may not necessarily enhance diversification rates. In fact, we hypothesise that overly specialised cases of myrmecophytism may even be an evolutionary dead end.