Cuckoo Fungus Mimics Termite Eggs by Producing the Cellulose-Digesting Enzyme β-Glucosidase

Abstract

Insects and fungi share a long history of association in various habitats, including the wood-decomposition niche. Fungal mimicry of termite eggs is one of the most striking evolutionary consequences of insect-fungus association. Termites of the genus Reticulitermes often harbor fungal sclerotia, called "termite balls," along with eggs in nursery chambers, whereby the fungus gains a competitor-free habitat in termite nests. Sophisticated morphological and chemical camouflage are needed for the fungus to mimic termite eggs. However, the mechanism of chemical egg mimicry by the fungus is unknown. Here, we show that the fungus mimics termite eggs chemically by producing the cellulose-digesting enzyme beta-glucosidase. We found that the termite egg-recognition pheromone consists of beta-glucosidase and lysozyme. Both enzymes are major salivary compounds in termites and are also produced in termite eggs. Termite balls were tended by termites only when the fungus produced beta-glucosidase. Our results demonstrated that the overlap of the cellulose digestion niche between termites and the fungus sharing the same chemicals provided the opportunity for the origin of termite egg mimicry by the fungus. This suggests that pheromone compounds might have originally evolved within other life history contexts, only later gaining function in chemical communication.