Detritivory, coprophagy, and the evolution of digestive mutualisms in Dietyoptera

We review literature on extant detritivores, including cockroaches and termites, and conclude that coprophagy was the key behavior leading to the evolution of hindgut fermentation systems in the stem group of Dictyoptera. Coprophagy exploits concentrated microbial consortia on cellulose based substrates. These microbes are potential mutualists and food, but they also initiate degradation of cellulose, detoxify allelochemicals and soften the substrate, a phenomenon known as the "external rumen". We suggest that the evolution of a sophisticated hindgut fauna is a process of internalizing this self-assembled microbial community, accompanied by changes in host-microbe interdependence, the source of microbial inoculum for neonates, and host social behavior. Proctodeal trophallaxis evolved from pre-existing intraspecific coprophagous behavior when termite ancestors became subsocial, because the physiology of encystment in oxymonad and hypermastigid flagellates precludes their transfer via cysts in adult feces. The behavior was reinforced by the benefits of using the trophic stages of flagellates as food. The association of these flagellates with the dictyopteran lineage is an ancient one, and may have originated as part of the external rumen in the Carboniferous coal swamps.