The evolutionary history of the attine ant-fungus symbiosis: Phylogenetic analyses of attine ants (Formicidae: Attini) and their fungi (Basidiomycotina: Lepiotaceae and Tricholomataceae) using morphological and molecular characters

The evolutionary history of the symbiosis between fungus-growing ants (subfamily Myrmicinae, tribe Attini) and their fungi is elucidated by inferring and comparing the phylogenies of both symbionts.; Both morphological and molecular data are utilized for the ant phylogeny. Forty-four morphological characters (109 states) of the prepupal worker larva are defined and analyzed for 51 attine species (representing 11 of the 12 currently recognized attine genera, and excluding only the monotypic workerless parasite Pseudoatta) and 16 non-attine species. DNA sequence data from the mitochondrial cytochrome oxidase I and II gene regions, as well as from the intervening tRNA leucine region, are analyzed for 12 species of attine ants and 1 outgroup species. Sequence data from the nuclear 28S ribosomal DNA region are analyzed for 21 fungal strains isolated from the nests of 19 attine species, as well as for 16 species of basidiomycete fungi not associated with attine ants.; The results indicate that the fungus-growing behavior had a single evolutionary origin in the ants. They also indicate that, contrary to the prevailing notion, mycelium cultivation is primitive and yeast cultivation is derived within the Attini. Though a monophyletic group of ants cultivate fungi, those fungi are polyphyletic, i.e., they represent several distinct lineages that are not closely related. Most ant-cultivated fungi belong to the basidiomycete family Lepiotaceae; however, one ant genus, Apterostigma, has acquired a distantly related basidiomycete lineage. Phylogenetic patterns suggest that some primitive attines may have repeatedly acquired lepiotaceous symbionts. In contrast, clonal inheritance of the same fungal lineage over at least the past 23 million years is the most likely explanation for the pattern of fungus and ant relationships in the most derived attines.