Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts

Abstract

Adaptation to different resources has the potential to cause rapid species diversification, but few studies have been able to quantify the time scale of recent adaptive radiations. The pea aphid, Acyrthosiphon pisum, a model of speciation for host-specialized parasites, consists of several biotypes (races or species) living on distinct legume hosts. To document this radiation, we used rapidly evolving sequences from Buchnera, the maternally transmitted bacterial endosymbiont of aphids. Analyses of Buchnera pseudogene sequences revealed that 11 host-associated biotypes sort mostly into distinct matrilines despite low sequence divergence. A calibration based on divergence times of 7 sequenced genomes of Buchnera allowed us to date the last maternal ancestor of these biotypes between 8,000 and 16,000 years, with a burst of diversification at an estimated 3,600-9,500 years. The recency of this diversification, which is supported by microsatellite data, implies that the pea aphid complex ranks among the most rapid adaptive radiations yet documented. This diversification coincides with post-Pleistocene warming and with the domestication and anthropogenic range expansion of several of the legume hosts of pea aphids. Thus, we hypothesize that the new availability or abundance of resources triggered a cascade of divergence events in this newly formed complex.