Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mitochondrial and nuclear loci.

Termites of the genus Reticulitermes are ecologically and economically important wood-feeding social insects that are widespread in the Holarctic region. Despite their importance, no study has yet attempted to reconstruct a global time-scaled phylogeny of Reticulitermes termites. In this study, we sequenced mitochondrial (2096bp) and nuclear (829bp) loci from 61 Reticulitermes specimens, collected across the genus' entire range, and one specimen of Coptotermes formosanus, which served as an outgroup. Bayesian and Maximum likelihood analyses conducted on the mitochondrial and nuclear sequences support the existence of four main lineages that span four global geographical regions: North America (NA lineage), western Europe (WE lineage), a region including eastern Europe and western Asia (EA+WA lineage), and eastern Asia (EA lineage). The mitochondrial data allowed us to clarify the phylogenetic relationships among these lineages. They were also used to infer a chronogram that was time scaled based on age estimates for termite fossils (including the oldest Reticulitermes fossils, which date back to the late Eocene-early Oligocene). Our results support the hypothesis that the extant Reticulitermes lineage first differentiated in North America. The first divergence event in the ancestral lineage of Reticulitermes occurred in the early Miocene and separated the Nearctic lineages (i.e., the NA lineages) from the Palearctic lineages (i.e., WE, EE+WA, and EA lineages). Our analyses revealed that the main lineages of Reticulitermes diversified because of vicariance and migration events, which were probably induced by major paleogeographic and paleoclimatic changes that occurred during the Cenozoic era. This is the first global and comprehensive phylogenetic study of Reticulitermes termites, and it provides a crucial foundation for studying the evolution of phenotypic and life-history traits in Reticulitermes. For instance, the phylogeny we obtained suggested that 'asexual queen succession', a unique reproductive system, independently evolved at least three times during the diversification of the genus.