Abstract
In the African and Asian tropics, termites of the subfamily Macrotermitinae play a major role in the decomposition of dead plant material. Their ecological success lies in the obligate mutualism of the termites with fungi of the genus Termitomyces. Before the advent of molecular studies, the interaction with these fungi was poorly understood. Here, we combined available ITS sequence data from West, Central, and South Africa with data of 39 new samples from East Africa to achieve the most comprehensive view of the diversity and host specificity of Termitomyces symbionts across Africa to date. A high amount of sequence divergence in the ITS sequences was found; 11 different Termitomyces lineages in East Africa and >30 lineages across Africa were identified, and the expected diversity is estimated to be about 41 lineages. The fungal lineages belong to four major clades, each almost exclusively associated with one termite host genus. Analysis of molecular variance revealed that 40% of the ITS sequence variation occurred between host genera, indicating close co-evolution at this level. However, within host genera, fungal lineages and haplotypes were frequently shared among host species and sampling localities, except for fungal symbionts of Odontotermes. Horizontal transmission of fungal symbionts may facilitate the transfer of haplotypes and species among hosts. However, at present, we have little understanding of the maintenance of specificity at the genus level. Possible explanations range from substrate specificity of fungi to an active selection of fungi by termites.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Aanen D.K. 2006. As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi. Biol. Lett. 2: 209-212
Aanen D.K. and Boomsma J.J. 2006a. The evolutionary origin and maintenance of the mutualistic symbiosis between termites and fungi. In: Insect Symbiosis vol. 2 (Miller T. and Bourtzis K., Eds), CRC Press, London, pp 79-95
Aanen D.K. and Boomsma J.J. 2006b. Evolutionary dynamics of the mutualistic symbiosis between fungus-growing termites and Termitomyces fungi. In: Insect-Fungal Associations: Ecology and Evolution (Vega F. and Blackwell M., Eds), Oxford University Press, Oxford, pp 191-210
Aanen D.K. and Eggleton P. 2005. Fungus-growing termites originated in African rain forest. Curr. Biol. 15: 851-855
Aanen D.K., Eggleton P., Rouland-Lefèvre C., Frøslev T.G. and Rosendahl S. 2002. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl. Acad. Sci. USA 99: 14887-14892
Aanen D.K., Ros V.I.D., de Fine Licht H.H., Mitchell J., de Beer Z.W., Slippers B., Rouland-Lefèvre C. and Boomsma J.J. 2007. Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evol. Biol. 7: 115
Aanen D.K., de Fine Licht H.H., Debets A.J.M., Kerstes N.A.G., Hoekstra R.F. and Boomsma J.J. 2009. High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 326: 1103-1106
Arnold A.E. and Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541-549
Bignell D.E. 2000. Symbiosis with fungi. In: Termites: Evolution, Sociality, Symbioses, Ecology (Abe T., Bignell D.E. and Higashi M., Eds), Kluwer Academic Publishers, Dordrecht, pp 189-208
Bingham M.G. 2002. Are species of Termitomyces specific to their host termites? Kirkia 18: 77-82
Buxton R.D. 1981. Termites and the turnover of dead wood in an arid tropical environment. Oecologia 51: 379-384
Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11: 265-270
Collins N.M. 1981. The role of termites in the decomposition of wood and leaf litter in the Southern Guinea savanna of Nigeria. Oecologia 51: 389-399
Darlington J.P.E.C. 1994. Nutrition and evolution in fungus-growing termites. In: Nourishment and Evolution in Insect Societies (Hunt J.H. and Nalepa C.A., Eds), Westview Press, Boulder, pp 105-130
de Fine Licht H.H., Andersen A. and Aanen D.K. 2005. Termitomyces sp. associated with the termite Macrotermes natalensis has a heterothallic mating system and multinucleate cells. Mycol. Res. 109: 314-318
de Fine Licht H.H., Boomsma J.J. and Aanen D.K. 2006. Presumptive horizontal symbiont transmission in the fungus-growing termite Macrotermes natalensis. Mol. Ecol. 15: 3131-3138
de Fine Licht H.H., Boomsma J.J. and Aanen D.K. 2007. Asymmetric interaction specificity between two sympatric termites and their fungal symbionts. Ecol. Entomol. 32: 76-81
deMenocal P.B. 2004. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet. Sci. Lett. 220: 3-24
Excoffier L.G.L. and Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50
Felsenstein J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Mol. Evol. 46: 368-376
Frøslev T.G., Aanen D.K., Læssøe T. and Rosendahl S. 2003. Phylogenetic relationships of Termitomyces and related taxa. Mycol. Res. 107: 1277-1286
Frøslev T.G., Jeppesen T.S., Læssøe T. and Kjøller R. 2007. Molecular phylogenetics and delimitation of species in Cortinarius section Calochroi (Basidiomycota, Agaricales) in Europe. Mol. Phylogenet. Evol. 44: 217-227
Gardes M. and Bruns T.D. 1996. ITS-RFLP matching for identification of fungi. In: Species Diagnostics Protocols: PCR and Other Nucleic Acid Methods (Clapp J.P., Ed), Humana Press Inc., Totowa, NJ, pp 177-186
Gotelli N.J. and Entsminger G.L. 2004. EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT. http://garyentsminger.com/ecosim/index.htm
Grassé P.P. and Noirot C. 1955. La fondation de nouvelles sociétés par Bellicositermes natalensis (Hav.). Insect. Soc. 2: 213-220
Härkönen M., Saarimäki T. and Mwasumbi L. 1995. Edible mushrooms of Tanzania. Karstenia 35 Suppl.: 92
Hasegawa M., Kishino H. and Yano T.-A. 1985. Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160-174
Heim R. 1977. Termites et Champignons. Les Champignons Termitophiles d′Afrique Noire et d′Asie Méridionale. Société Nouvelle des Éditions Boubée, Paris, 205 pp
Hibbett D.S., Tsuneda A., Fukumasa-Nakai Y. and Donoghue M.J. 1995. Phylogenetic diversity in shiitake inferred from nuclear ribosomal DNA sequences. Mycologia 87: 618-638
Hyodo F., Tayasu I., Inoue T., Azuma J.-I. and Kudo T. 2003. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct. Ecol. 17: 186-193
Johnson R.A. 1981. Colony development and establishment of the fungus comb in Microtermes sp. nr. usambaricus (Sjöstedt) (Isoptera: Macrotermitinae) from Nigeria. Insect. Soc. 28: 3-12
Johnson R.A., Thomas R.J., Wood T.G. and Swift M.J. 1981. The inoculation of the fungus comb in newly founded colonies of some species of the Macrotermitinae (Isoptera) from Nigeria. J. Nat. Hist. 15: 751-756
Kambhampati S. and Eggleton P. 2000. Taxonomy and phylogeny of termites. In: Termites: Evolution, Sociality, Symbioses, Ecology (Abe T., Bignell D.E. and Higashi M., Eds), Kluwer Academic Publishers, Dordrecht, pp 1-23
Katende A.B., Segawa P., Birnie A., Holding C. and Tengnas B. 1999. Wild Food Plants And Mushrooms of Uganda. Regional Land Management Unit/Sida, Nairobi, Kenya, 490 pp
Katoh H., Miura T., Maekawa K., Shinzato N. and Matsumoto T. 2002. Genetic variation of symbiotic fungi cultivated by the macrotermitine termite Odontotermes formosanus (Isoptera: Termitidae) in the Ryukyu Archipelago. Mol. Ecol. 11: 1565-1572
Katoh K., Asimenos G. and Toh H. 2009. Multiple alignment of DNA sequences with MAFFT. In: Bioinformatics for DNA Sequence Analysis (Posada D., Ed), Humana Press, Totowa, NJ, pp 39-64
Kirk P.M., Cannon P.F., Minter D.W. and Stalpers J.A. 2008. Ainsworth & Bisby′s Dictionary of the Fungi, 10th ed. CABI Publishing, Wallingford, 771 pp
Korb J. and Aanen D.K. 2003. The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae). Behav. Ecol. Sociobiol. 53: 65-71
Lynch M.D.J. and Thorn R.G. 2006. Diversity of basidiomycetes in Michigan agricultural soils. Appl. Environ. Microbiol. 72: 7050-7056
Maddison W.P. and Maddison D.R. 2009. Mesquite: a modular system for evolutionary analysis. Version 2.6. http://mesquiteproject.org
Martin M.M. and Martin J.S. 1978. Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: The role of acquired digestive enzymes. Science 199: 1453-1455
Minin V., Abdo Z., Joyce P. and Sullivan J. 2003. Performance-based selection of likelihood models for phylogeny estimation. Syst. Biol. 52: 674-683
Moriya S., Inoue T., Ohkuma M., Taprab Y., Johjima T., Suwanarit P., Sangwanit U., Vongkaluang C., Noparatnaraporn N. and Kudo T. 2005. Fungal community analysis of fungus gardens in termite nests. Microbes Environ. 20: 243-252
Müller K. 2005. SeqState: Primer design and sequence statistics for phylogenetic DNA datasets. Appl. Bioinf. 4: 65-69
Nobre T., Eggleton P. and Aanen D.K. 2010. Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites? Proc. R. Soc. B 277: 359-365
Nylander J.A.A. 2004. MrModeltest v2. distributed by the author, Evolutionary Biology Center, Uppsala University
Ohiagu C.E. and Wood T.G. 1979. Grass production and decomposition in Southern Guinea savanna, Nigeria. Oecologia 40: 155-165
Oksanen J., Kindt R., Legendre P., O’Hara B., Simpson G.L. and Stevens H.H. 2008. vegan: Community ecology package. R package version 1.11-4. http://vegan.r-forge.r-project.org
Otieno N.C. 1964. Contributions to a knowledge of termite fungi in East Africa. Proc. East African Acad. 2: 109-121
Otieno N.C. 1968. Further contributions to a knowledge of termite fungi in East Africa. Sydowia 22: 160-165
Pegler D.N. 1977. A Preliminary Agaric Flora of East Africa. Lubrecht & Cramer Ltd, London, 620 pp
Pomeroy D.E., Bagine R.K. and Darlington J.P.E.C. 1991. Fungus-growing termites in East African savannas. In: African Wildlife: Research and Management (Kayanja F.I.B. and Edroma E.L., Eds), ICSU Press, Paris, pp 41-50
R Development Core Team 2008. R: language and environment for statistical computing. R version 2.7.0. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Rohrmann G.F. 1978. The origin, structure, and nutritional importance of the comb in two species of Macrotermitinae (Insecta, Isoptera). Pedobiol. 18: 89-98
Ronquist F. and Huelsenbeck J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinf. 19: 1572-1574
Rouland-Lefèvre C. 2000. Symbiosis with fungi. In: Termites: Evolution, Sociality, Symbioses, Ecology (Abe T., Bignell D.E. and Higashi M., Eds), Kluwer Academic Publishers, Dordrecht, pp 289-306
Rouland C., Lenoir F. and Lepage M. 1991. The role of the symbiotic fungus in the digestive metabolism of several species of fungus-growing termites. Comp. Biochem. Physiol. A 99: 657-663
Rouland-Lefèvre C., Diouf M.N., Brauman A. and Neyra M. 2002. 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. Mol. Phylogenet. Evol. 22: 423-429
Sands W.A. 1960. The initiation of fungus comb construction in laboratory colonies of Ancistrotermes guineensis (Silvestri). Insect. Soc. 7: 251-263
Sands W.A. 1969. The association of termites and fungi. In: Biology of Termites, vol. 1 (Krishna K. and Weesner F.M., Eds), Academic Press, London, pp 495-524
Schuurman G. 2005. Decomposition rates and termite assemblage composition in semiarid Africa. Ecology 86: 1236-1249
Shinzato N., Muramatsu M., Watanabe Y. and Matsui T. 2005. Termite-regulated fungal monoculture in fungus combs of a macrotermitine termite Odontotermes formosanus. Zool. Sci. 22: 917-922
Sidde Gowda D.K. and Rajagopal D. 1990. Association of Termitomyces spp. with fungus growing termites. Proc. Ind. Acad. Sci. (Anim. Sci.) 99: 311-315
Sieber R. 1983. Establishment of fungus comb in laboratory colonies of Macrotermes michaelseni and Odontotermes montanus (Isoptera, Macrotermitinae). Insect. Soc. 30: 204-209
Simmons M.P. and Ochoterena H. 2000. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 49: 369-381
Swofford D.L. 2001. PAUP* Vers. 4.0b10. Sinauer, Sunderland, MA
Tamura K., Dudley J., Nei M. and Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599
Taprab Y., Ohkuma M., Johjima T., Maeda Y., Moriya S., Inoue T., Suwanarit P., Noparatnaraporn N. and Kudo T. 2002. Molecular phylogeny of symbiotic Basidiomycetes of fungus-growing termites in Thailand and their relationship with the host. Biosci. Biotechnol. Biochem. 66: 1159-1163
Thomas R.J. 1987. Factors affecting the distribution and activity of fungi in the nests of Macrotermitinae. Soil Biol. Biochem. 19: 343-349
White T.J., Bruns T., Lee S. and Taylor L. 1990. Amplification and direct sequencing of fungal RNA genes for phylogenetics. In: PCR Protocols. A Guide to Methods and Applications (Innis M.A., Gelfand D.H., Sninsky J.J. and White T.J., Eds), Academic Press, San Diego,CA, pp 315-322
Wilfert L., Kaib M., Durka W. and Brandl R. 2006. Differentiation between populations of a termite in eastern Africa: Implications for forest biogeography. J. Biogeogr. 33: 1993-2000
Wood T.G. and Thomas R.J. 1989. The mutualistic association between Macrotermitinae and Termitomyces. In: Insect-Fungus Interactions (Wilding N., Hammond P.M. and Webber J.F., Eds), Academic Press, London, pp 69-92
Acknowledgments
The study was supported by the German Research Foundation (DFG). Zipporah Osiemo was supported by a scholarship of the German Academic Exchange Service (DAAD). We thank Duur K. Aanen for valuable comments on an earlier version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Z. B. Osiemo and A. Marten contributed equally to this work.
Rights and permissions
About this article
Cite this article
Osiemo, Z.B., Marten, A., Kaib, M. et al. Open relationships in the castles of clay: high diversity and low host specificity of Termitomyces fungi associated with fungus-growing termites in Africa. Insect. Soc. 57, 351–363 (2010). https://doi.org/10.1007/s00040-010-0092-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-010-0092-3