Molecular Phylogenetic Study of a Myrmecophyte Symbiosis: DidLeonardoxa/Ant Associations Diversify via Cospeciation?

Abstract

TheLeonardoxa africana(Leguminosae: Caesalpinioideae) complex is a group of four closely related taxa (L1 to L4) exhibiting various grades of specificity and specialization in mutualistic associations with ants. Each of the two most specialized species,Leonardoxataxon 3 (L3) andL. africanasensu stricto (L4), interacts with a specific species of formicine ant, respectivelyAphomomyrmex aferandPetalomyrmex phylax,which nests in specialized swollen twigs. These two monotypic genera are the sole African members of the tribe Myrmelachistini, and their occurrence in closely related plants suggested the hypothesis that the two associations L4/Petalomyrmexand L3/Aphomomyrmexare derived by cospeciation from an ancestral association. Phylogenies based on DNA sequences were reconstructed for the ants and compared with phylogenies available for the plants in order to test for this hypothesis of cospeciation. The resulting topologies suggest either that the association with myrmelachistine ants arose several times or that a plant species (L2) and an ant population split off from an ancestral association. Furthermore, dates of speciation events appear to differ between ants and corresponding plants. An estimate of at least 4 million years was obtained for the separation ofAphomomyrmexandPetalomyrmex,whereas biological, biogeographic, and molecular–genetic data suggest a much more recent divergence for the plants. Thus, we reject the hypothesis of cospeciation and conclude thatAphomomyrmexandPetalomyrmexindependently colonized different taxa ofLeonardoxa.This striking instance of parallel evolution supports the notion that specific ant–plant associations originated by ecological fitting of preadapted partners. We discuss alternative evolutionary scenarios that are consistent with molecular data.