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.
Background: Termites of the subfamily Macrotermitinae live in a mutualistic symbiosis with basidiomycete fungi of the genus Termitomyces. Here, we explored interaction specificity in fungus-growing termites using samples from 101 colonies in South-Africa and Senegal, belonging to eight species divided over three genera. Knowledge of interaction specificity is important to test the hypothesis that inhabitants (symbionts) are taxonomically less diverse than 'exhabitants' (hosts) and to test the hypothesis that transmission mode is an important determinant for interaction specificity.
Abstract:Associations between termites and fungi are considered in two categories: firstly, interactions that affect the discovery and consumption of food or its nutrient value, but which fall short of mutualism; secondly, the cultivation of fungus-combs (Termitomyces spp.) within the nesting system by Macrotermitinae, where there is an obligate reliance on the fungus and which in most cases appears to contribute to the degradation of plant structural compounds, especially xylans. In the first category most information is available for pest termites and it is possible to show, in different species or circumstances, roles for fungal colonizers of decaying wood (or for their metabolic products) as attractants, repellents, conditioners, toxins, and nutritional supplements. Some entomophagous fungi are pathogenic to termites and may be potential agents of biological control, despite low host specificities. In the second category of association, the structures and dynamics of Macrotermitine fungus-combs are classified and data presented to illustrate the variety of net enzymatic synergisms (i.e. [mal hydrolytic activities and specificities in the termite gut) achieved by the mutualism in different host species and feeding groups. To reconcile the conflicting evidence on possible enzyme acquisition from the fungus by the termite, it is proposed that symbiosis in the Macrotermitinae shows evolutionary diversification, with some species of fungus producing a range of enzymes according to substrate and enviromnental conditions (generalists), others with a fixed range of enzymes not responsive to substrate (constitutive specialists) and yet others which produce little, if any, enzyme for termite use. The assay of enzyme productions in pure cultures of Termitomyces, and the host specificities of different species of the fungal partner are also reviewed.
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