The Evolution of Insect-Fungus Associations: From Contact to Stable Symbiosis

Abstract

Insect-fungus interactions range from agonistic to mutualistic, and include several spectacular examples of complex symbioses. A potential benefit of mycophagy (the ingestion of fungal tissue) is the augmentation of digestive capacity by the ingestion of fungal enzymes that remain active in the gut following ingestion. Cellulose digestion is mediated by ingested fungal enzymes in the wood-boring larvae of cerambycid beetles and siricid woodwasps, in detritus-feeding stonefly nymphs, and in the workers of fungus-growing termites. In this paper I discuss a plausible scenario for the evolution of stable symbiotic insect-fungus associations, in which the augmentation of digestive capacity through the ingestion of fungal enzymes is an important factor leading to the establishment of interdependence between the interacting partners in a mutualism. Ingested fungal enzymes play a different role in the mutualistic association of the attine ants and their symbiotic fungi. Analyses of the associations of the siricid woodwasps, fungus-growing termites, and fungus-growing ants with their symbiotic fungi permit the testing of Law's (1985) predictions concerning the consequences of evolution in a mutualistic environment. As predicted, the rate of speciation has been slower in the protected partner than in the host partner, selection has favored asexual reproduction in the protected partner, and, at least in the attine ant-fungus symbiosis, the protected partner exhibits a low degree of specificity toward different host species. Insect-fungus interactions provide rich material for the study of both mechanistic and theoretical aspects of mutualism.