Whole genome data reveal the complex history of a diverse ecological community

How widespread ecological communities assemble remains a key question in ecology. Trophic interactions between widespread species may reflect a shared population history, or ecological sorting of local pools of species with very different population histories. Which scenario applies is central to the stability of trophic associations, and the potential for coevolution between species. Here we show how alternative community assembly hypotheses can be discriminated using whole genome data for component species, and provide a novel likelihood framework that overcomes current limitations in formal comparison of multispecies histories. We illustrate our approach by inferring the assembly history of a Western Palaearctic community of insect herbivores and parasitoid natural enemies, trophic groups that together comprise 50% of terrestrial species. We reject models of co-dispersal from a shared origin, and of delayed enemy pursuit of their herbivore hosts, arguing against herbivore attainment of ‘enemy-free space’. The community-wide distribution of species expansion times is also incompatible with a random, neutral model of assembly. Instead, we reveal a complex assembly history of single- and multi-species range expansions through the Pleistocene from different directions and over a range of timescales. Our results suggest substantial turnover in species associations, and argue against tight coevolution in this system. The approach we illustrate is widely applicable to natural communities of non-model species, and makes it possible to reveal the historical backdrop against which selection acts.