Explosive Adaptive Radiation and Extreme Phenotypic Diversity within Ant-Nest Beetles

Summary Ant-nest beetles (Paussus) are the quintessential Trojan horses of the insect world. They hack the complex communication system of ants, allowing them to blend into the ant society and be treated as royalty, all the while preying upon the ants and the ants’ brood and duping the ants into rearing their young [1–3]. Here we present results of the first molecular-based phylogeny of ant-nest beetles, which reveals that this symbiosis has produced one of the most stunning examples of rapid adaptive radiation documented to date. The most recent ancestor of a Paussus clade endemic to Madagascar is only 2.6 million years old. This species gave rise to a remarkably phenotypically diverse clade of 86 extant species with a net diversification interval of 0.38–0.81 million years, a rate of radiation faster than classic textbook examples of large, recent, rapid radiations such as Anolis lizards on Caribbean islands, cichlids of the East African Great Lakes, finches on the Galápagos Islands, and Drosophila and tetragnathid spiders on the Hawaiian Islands [4–8]. In order for Paussus to adapt to a new host ant species, the beetle’s ability to perceive, deceive, and communicate with the new host must evolve quickly and in synchrony in both the larval and adult life stages, resulting in unusually strong selective pressure levied by their host ants. Data on host associations suggest that the history of host shifts may help explain both the striking phenotypic diversity within the Malagasy radiation and the evolution of phenotypically similar yet distantly related species in Madagascar and Africa.