Deep-Time Convergence in Rove Beetle Symbionts of Army Ants

Recent adaptive radiations provide striking examples of convergence [1–4], but the predictability of evolution over much deeper timescales is controversial, with a scarcity of ancient clades exhibiting repetitive patterns of phenotypic evolution [5, 6]. Army ants are ecologically dominant arthropod predators of the world's tropics, with large nomadic colonies housing diverse communities of socially parasitic myrmecophiles [7]. Remarkable among these are many species of rove beetle (Staphylinidae) that exhibit ant-mimicking “myrmecoid” body forms and are behaviorally accepted into their aggressive hosts’ societies: emigrating with colonies and inhabiting temporary nest bivouacs, grooming and feeding with workers, but also consuming the brood [8–11]. Here, we demonstrate that myrmecoid rove beetles are strongly polyphyletic, with this adaptive morphological and behavioral syndrome having evolved at least 12 times during the evolution of a single staphylinid subfamily, Aleocharinae. Each independent myrmecoid clade is restricted to one zoogeographic region and highly host specific on a single army ant genus. Dating estimates reveal that myrmecoid clades are separated by substantial phylogenetic distances—as much as 105 million years. All such groups arose in parallel during the Cenozoic, when army ants diversified into modern genera [12] and rose to ecological dominance [13, 14]. This work uncovers a rare example of an ancient system of complex morphological and behavioral convergence, with replicate beetle lineages following a predictable phenotypic trajectory during their parasitic adaptation to host colonies.