Molecular phylogenetic study of a myrmecophyte symbiosis: did Leonardoxa/ ant associations diversify via cospeciation?

The Leonardoxa 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, Leonardoxa taxon 3 (L3) and L. africana sensu stricto (L4), interacts with a specific species of formicine ant, respectively Aphomomyrmex after and Petalomyrmex 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 thehypothesis that the two associations L4/Petalomyrmex and L3/Aphomomyrmex are 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 of Aphomomyrmex and Petalomyrmex, 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 that Aphomomyrmex and Petalomyrmex independently colonized different taxa of Leonardoxa. 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.