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, 99 (23), 14887-92

The Evolution of Fungus-Growing Termites and Their Mutualistic Fungal Symbionts

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The Evolution of Fungus-Growing Termites and Their Mutualistic Fungal Symbionts

Duur K Aanen et al. Proc Natl Acad Sci U S A.

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 free-living state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite species can have different symbionts. Data are consistent with horizontal transmission of fungal symbionts in both the ancestral state of the mutualism and most of the extant taxa. Clonal vertical transmission of fungi, previously shown to be common in the genus Microtermes (via females) and in the species Macrotermes bellicosus (via males) [Johnson, R. A., Thomas, R. J., Wood, T. G. & Swift, M. J. (1981) J. Nat. Hist. 15, 751-756], 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.

Figures

Fig 1.
Fig 1.
Majority-rule consensus trees of fungus-growing termites (Left) and their fungal symbionts (Right) of trees sampled in a Bayesian analysis. The numbers above the branches refer to the Bayesian posterior probability of the nodes (>50%) and were derived from 28,000 Markow chain Monte Carlo-sampled trees. Three independent Markow chain Monte Carlo runs, each starting with random trees for each of four simultaneous chains, resulted in concordant joint posterior probability distributions for the topologies. Alternative estimations based on maximum-likelihood were almost identical. The values below branches represent percent support in maximum-likelihood nonparametric bootstrapping. Termites and their corresponding fungal symbionts are connected by thin lines. The five major termite clades, labeled A–E, and their corresponding fungal symbionts are indicated with different colors to illustrate the degree of specificity. Exceptions to this pattern of higher-level specificity are indicated in black. The two termite clades with vertical uniparental symbiont transmission [by different sexes as indicated (7, 8)] are contained in gray boxes, whereas yellow boxes indicate the two termite clades and five fungal clades from Asia. Termites for which we were not able to obtain one or both fungal DNA sequences are indicated with an asterisk. Sequences derived from herbarium basidiocarps of seven fungal morphospecies were included to link a number of termite symbionts with known strains of Termitomyces. Mi, Microtermes; An, Ancistrotermes; Sy, Synacanthotermes; Ma, Macrotermes; Od, Odontotermes; Hy, Hypotermes; Pr, Protermes; Ps, Pseudacanthotermes; Ac, Acanthotermes; Fo, Foraminitermes; and La, Labritermes.

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