Ancestral Predisposition Towards a Domesticated Lifestyle in the Termite-Cultivated Fungus <i>Termitomyces</i>

Abstract

The ancestor of termites relied on gut symbionts for degradation of plant material, an association that persists in most termite families. However, the single lineage Macrotermitinae has additionally acquired a fungal symbiont that complements digestion of food outside the termite gut. Phylogenetic analysis has shown that fungi grown by these termites form a monophyletic group – the genus Termitomyces , but the events leading towards domestication remain unclear . To address this, we reconstructed the lifestyle of the common ancestor of Termitomyces using a combination of ecological data with a phylogenomic analysis of 21 related non-domesticated species and 25 species of Termitomyces. We show that the closely related genera Blastosporella and Arthromyces also contain insect-associated species. We demonstrate that the genus Arthromyces produces asexual spores on the mycelium, which may facilitate their dispersal by insects when growing on aggregated subterranean faecal pellets of a plant-feeding insect. The sister relationship between Arthromyces and Termitomyces implies that insect-association and asexual sporulation, which are present in both genera, preceded the domestication of Termitomyces and did not follow domestication as has been proposed previously. Specialisation of the last common ancestor of these two genera on an insect-faecal substrate is further supported by similar carbohydrate-degrading profiles between Arthromyces and Termitomyces. We describe a ‘termite-domestication syndrome’, with each component found scattered in related genera and species outside of the termite-domesticated clade. This pattern indicates that the origin of the termite-fungus symbiosis may not have required large-scale changes of the fungal partner.