The Termite Worker Phenotype Evolved as a Dispersal Strategy for Fertile Wingless Individuals before Eusociality

Termites are eusocial insects that evolved from solitary cockroaches. It is not known precisely what factors drove the evolution of termite eusociality, that is, skewed reproduction with distinct winged reproductive and wingless worker phenotypes. In other eusocial insects (bees and wasps), reproductive skew evolved first and phenotype differences evolved second. We propose that the reverse pattern occurred in termites, that is, that the winged-wingless diphenism evolved before eusociality. We discuss existing phylogenetic and pheromonal evidence supporting our hypothesis. We provide new experimental evidence from the most basal termite species (Mastotermes darwiniensis), suggesting that the ancestral state was indeed diphenic but presocial. We propose that the mechanism promoting a winged-wingless diphenism-in the absence of eusociality-was greater predation of aerial than terrestrial dispersers, and we support this with a game theoretic model. We augment our hypothesis with a novel explanation for the evolution of the developmental pathways leading to winged and wingless phenotypes in termites. An added benefit of our hypothesis is that it neatly explains the origin of termite eusociality itself: in the pre-eusocial ancestral species, the poor dispersal ability of the wingless phenotype would have led to clustering of relatives around shared resources-a prerequisite for nonparental care of close relatives.