The evolution of fungus-growing termites and their mutualistic fungal symbionts

Abstract

We have estimated phylogenies of fungus-growing termites and their associated mutualistic fungi of the genus Termitomyces using Bayesian analyses of DNA sequences. Our study shows that the symbiosis has a single African origin and that secondary domestication of other fungi or reversal of mutualistic fungi to a freeliving state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite , is derived with two independent origins. Despite repeated host switching, statistical tests taking phylogenetic uncertainty into account show a significant congruence between the termite and fungal phylogenies, because mutualistic interactions at higher taxonomic levels show considerable specificity. We identify common characteristics of fungus-farming evolution in termites and ants, which apply despite the major differences between these two insect agricultural systems. We hypothesize that biparental colony founding may have constrained the evolution of vertical symbiont transmission in termites but not in ants where males die after mating.

As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi

“…This would imply that the fungal symbionts have not been selected to invest in antagonistic traits, but this prediction remains to be tested. The few studies that have addressed within-nest variation of fungal symbionts, have found single cultures within single nests (Aanen et al 2002;Katoh et al 2002), consistent with the hypothesis that recurrent bottlenecking within nests reduces fungal within-nest variation. However, more research is needed to confirm this hypothesis, especially for species with multiple separate fungus combs per nest.…”

Diversity, phenology and distribution of Termitomyces species in Côte d’Ivoire

“…They developed a sophisticated mutualistic symbiosis with a kind of fungi ( Termitomyces spp., Basidiomycotina), which they cultivate on combs constructed from faecal material within their nests (Johnson et al 1981; Wood and Thomas 1989). This symbiosis firstly occurred with no reversions to free-living states (Aanen et al 2002) at least 31 million years ago (Nobre et al 2011) and is obligate for both partners: the termites provide a constant, highly regulated growth environment for their fungal symbionts, while the fungi provide food for the termites. Fungi are cultivated on combs constructed from faecal material within termites’ nests (Wood and Thomas 1989).…”

Diversity, population genetics, and evolution of macrofungi associated with animals

“…Through horizontal transmission, a given fungal species can establish symbiotic relationship with several termite species within a genus (Aanen et al 2002). Evidence for the dominant role of horizontal transmission of Termitomyces genotypes has been found in sequence analyses of Termitomyces .…”

“…Furthermore, by analyzing the relationships between several termite species from Asia and their associated Termitomyces fungi, Taprab et al (2002) discovered that the symbiotic fungal species and their distribution paralleled those of the termites. Similarly, Aanen et al (2002) investigated 32 termite species in 9 genera from Asia and Africa and their associated Termitomyces fungi. The results showed that the symbiosis has a single African origin, with no evidence for secondary domestication of other fungi or the reversal of mutualistic fungi to a free-living state.…”

“…The results showed that the symbiosis has a single African origin, with no evidence for secondary domestication of other fungi or the reversal of mutualistic fungi to a free-living state. The two phylogenetic trees, one for termites and the other one for fungi, both showed five main clades with an one-to-one correspondence (Aanen et al 2002). Together, these studies suggest that major splits have occurred simultaneously in the termites and fungi in their long co-evolutionary process.…”