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

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.

[1]  R. J. Thomas,et al.  The inoculation of the fungus comb in newly founded colonies of some species of the Macrotermitinae (Isoptera) from Nigeria , 1981 .

[2]  Roderic D. M. Page,et al.  COMPONENT ANALYSIS: A VALIANT FAILURE? , 1990 .

[3]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[4]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[5]  A. Smith,et al.  Rooting molecular trees: problems and strategies , 1994 .

[6]  Ted R. Schultz,et al.  Evolutionary History of the Symbiosis Between Fungus-Growing Ants and Their Fungi , 1994, Science.

[7]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[8]  Joost A. Stalpers,et al.  Ainsworth and Bisby's dictionary of the fungi: 9th edition. , 1995 .

[9]  S. Frank.  Host–symbiont conflict over the mixing of symbiotic lineages , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  K. Crandall,et al.  Phylogeny Estimation and Hypothesis Testing Using Maximum Likelihood , 1997 .

[11]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[12]  U. Mueller,et al.  The evolution of agriculture in ants , 1998, Science.

[13]  安部 琢哉,et al.  Termites: Evolution, Sociality, Symbioses, Ecology , 2000, Springer Netherlands.

[14]  J. Moncalvo,et al.  Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. , 2000, Systematic biology.

[15]  U. Mueller,et al.  The Origin of the Attine Ant-Fungus Mutualism , 2001, The Quarterly Review of Biology.

[16]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[17]  S. Rehner,et al.  PARTIAL INCOMPATIBILITY BETWEEN ANTS AND SYMBIOTIC FUNGI IN TWO SYMPATRIC SPECIES OF ACROMYRMEX LEAF‐CUTTING ANTS , 2001, Evolution; international journal of organic evolution.

[18]  W. Murphy,et al.  Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics , 2001, Science.

[19]  A. Brauman,et al.  Phylogenetic relationships in Termitomyces (Family Agaricaceae) based on the nucleotide sequence of ITS: a first approach to elucidate the evolutionary history of the symbiosis between fungus-growing termites and their fungi. , 2002, Molecular phylogenetics and evolution.

[20]  T. Miura,et al.  Genetic variation of symbiotic fungi cultivated by the macrotermitine termite Odontotermes formosanus (Isoptera: Termitidae) in the Ryukyu Archipelago , 2002, Molecular ecology.

[21]  James E. Johnson,et al.  One hundred and seventeen clades of euagarics. , 2002, Molecular phylogenetics and evolution.

[22]  U. Mueller,et al.  Extensive exchange of fungal cultivars between sympatric species of fungus‐growing ants , 2002, Molecular ecology.