A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology

Abstract

The first comprehensive combined molecular and morphological phylogenetic analysis of the major groups of termites is presented. This was based on the analysis of three genes (cytochrome oxidase II, 12S and 28S) and worker characters for approximately 250 species of termites. Parsimony analysis of the aligned dataset showed that the monophyly of Hodotermitidae, Kalotermitidae and Termitidae were well supported, while Termopsidae and Rhinotermitidae were both paraphyletic on the estimated cladogram. Within Termitidae, the most diverse and ecologically most important family, the monophyly of Macrotermitinae, Foraminitermitinae, Apicotermitinae, Syntermitinae and Nasutitermitinae were all broadly supported, but Termitinae was paraphyletic. The pantropical genera Termes, Amitermes and Nasutitermes were all paraphyletic on the estimated cladogram, with at least 17 genera nested within Nasutitermes, given the presently accepted generic limits. Key biological features were mapped onto the cladogram. It was not possible to reconstruct the evolution of true workers unambiguously, as it was as parsimonious to assume a basal evolution of true workers and subsequent evolution of pseudergates, as to assume a basal condition of pseudergates and subsequent evolution of true workers. However, true workers were only found in species with either separate- or intermediate-type nests, so that the mapping of nest habit and worker type onto the cladogram were perfectly correlated. Feeding group evolution, however, showed a much more complex pattern, particularly within the Termitidae, where it proved impossible to estimate unambiguously the ancestral state within the family (which is associated with the loss of worker gut flagellates). However, one biologically plausible optimization implies an initial evolution from wood-feeding to fungus-growing, proposed as the ancestral condition within the Termitidae, followed by the very early evolution of soil-feeding and subsequent re-evolution of wood-feeding in numerous lineages.