Evolution of host-plant associations and biogeographic patterns on a global scale within the oak gall wasps

Abstract

Co-evolutionary interactions between insect herbivores and their host plants underlie much contemporary biodiversity and are vital to assembly of natural ecosystems. Assemblages of galls on oaks induced by Cynipini wasps (Hymenoptera: Cynipidae) occur across much of the Northern Hemisphere, their diversity peaking in the Nearctic and on white oaks (Quercus section Quercus). However, the evolutionary history of the clade has been debated with respect to geographic origins, direction and timings of dispersal events, and shifts in host plant associations. We examined these questions using a global-scale, 6-gene phylogeny of 430 Cynipini species and a dataset of their associated host plants encompassing all eight sections within Quercus plus five Fagaceae genera. Likelihood-based ancestral state reconstructions demonstrate a Nearctic origin of the Cynipini followed by repeated colonisations of the Palearctic via both westwards and eastwards dispersal. These inferences are robust to bias in taxon sampling across continents and the inclusion of Protobalandricus as the sister lineage to Cynipini sensu stricto. Likewise, the association with white oaks is probably ancestral and has been retained by many Cynipini lineages. However, host shifts to other sections within Quercus and related Fagaceae genera are widely distributed across the cynipid phylogeny. They are associated with both global-scale range shifts and within-bioregion exploitation of alternative hosts, and their frequency typically correlates with host-plant relatedness. These findings highlight the evolutionary success of cynipids on white oak hosts and the connectedness of continental assemblages of gall wasps over evolutionary time

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