Explosive Radiation of Ant Parasitic Butterflies During the Miocene Aridification of Africa

Abstract

Extremely spezialized life history strategies are sometimes seen as evolutionary dead-ends. The Afrotropical butterfly genus Lepidochrysops exhibits such a life history. All 137 species are known or assumed to be phyto-predaceous, with caterpillars feeding on plants for the first few instars and later switching to parasitizing ants in the Formicinae, either by consuming ant brood or being fed by the ants through trophallaxis. The only other butterflies that exhibit this phyto-predaceous life history are those in the Palaearctic genus Phengaris (= Maculinea), a group of only a bout 11 species whose caterpillars parasitize ants in the Myrmicinae. We hypothesize that the move into ant nests by species of Lepidochrysops was an adaptive response to the aridification of Africa during the Miocene that facilitated subsequent radiation. Ant colonies have the advantage of providing both shelter from threats like fire and desiccation, as well as a stable food source when vegetation is scarce or unpredictable. To evaluate this hypothesis, we inferred a time-calibrated phylogeny using >400 loci for Lepidochrysops and its closest, non-parasitic relatives. We showed that this clade originated with the emerging Miombo woodlands about 22 million years ago (Mya), and spread to drier biomes as they became available. The diversity of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in an abrupt extinction. In contrast, the phyto-predaceous Lepidochrysops lineage radiated rapidly from around 6.5 Mya when phyto-predation likely evolved, showing the importance of this innovation for diversification and survival during the intensifying aridification of Africa.