Comparative dating of attine ant and lepiotaceous cultivar phylogenies reveals coevolutionary synchrony and discord

American Naturalist

Volumn 175, Issue 6, 2010, Pages

  Mikheyev, Alexander S ^a   Mueller, Ulrich G ^a   Abbot, Patrick ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Acromyrmex; Atta; Attini; Coevolution; Lepiotaceae; Leucoagaricus

Indexed keywords

ANT; COEVOLUTION; CULTIVAR; HOST-SYMBIONT INTERACTION; MUSHROOM; MUTUALISM; PHYLOGENY; SYMBIONT; SYNCHRONY;

AGARICALES; ANIMAL; ANT; ARTICLE; GENETICS; PHYLOGENY; SYMBIOSIS;

AGARICALES; ANIMALS; ANTS; PHYLOGENY; SYMBIOSIS;

ACROMYRMEX; ATTA; ATTINI; FORMICIDAE; FUNGI; LEPIOTACEAE; LEUCOAGARICUS;

EID: 77952071124     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/652472     Document Type: Article

References (63)

1. Aanen, D. K., P. Eggleton, C. Rouland-LeFevre, T. Guldberg-Froslev, S. Rosendahl, and J. J. Boomsma. 2002. The evolution of fungusgrowing termites and their mutualistic fungal symbionts. Proceedings of the National Academy of Sciences of the USA 99: 14887-14892.
2. Aanen, D. K., V. I. D. Ros, H. H. de Fine Licht, J. Mitchell, Z. W. de Beer, B. Slippers, C. Rouland-LeFevre, and J. J. Boomsma. 2007. Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evolutionary Biology 7:115.
3. Bascompte, J., and P. Jordano. 2007. Plant-animal mutualistic networks: The architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics 38:567-593.
4. Bascompte, J., P. Jordano, and J. M. Olesen. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431-433.
5. Becerra, J. X. 2003. Synchronous coadaptation in an ancient case of herbivory. Proceedings of the National Academy of Sciences of the USA 100:12804-12807.
6. Bidartondo, M. I. 2005. The evolutionary ecology of mycoheterotrophy. New Phytologist 167:335-352.
7. Borowicz, V. A., and S. A. Juliano. 1991. Specificity in host fungus associations: do mutualists differ from antagonists? Evolutionary Ecology 5:385-392.
8. Bruns, T. D., M. I. Bidartondo, and D. L. Taylor. 2002. Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integrative and Comparative Biology 42:352-359.
9. Caldera, E. J., M. Poulsen, G. Suen, and C. R. Currie. 2009. Insect symbioses: a case study of past, present, and future fungus-growing ant research. Environmental Entomology 38:78-92.
10. Chapela, I. H., S. A. Rehner, T. R. Schultz, and U. G. Mueller. 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691-1694.
11. Clark, M. A., N. A. Moran, P. Baumann, and J. J. Wernegreen. 2000. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids ( Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54:517-525.
12. Clay, K., and C. Schardl. 2002. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160(suppl.):S99-S127.
13. Currie, C. R., and A. E. Stuart. 2001. Weeding and grooming of pathogens in agriculture by ants. Proceedings of the Royal Society B: Biological Sciences 268:1033-1039.
14. Currie, C. R., B. Wong, A. E. Stuart, T. R. Schultz, S. A. Rehner, U. G. Mueller, G.-H. Sung, J. W Spatafora, and N. A. Strauss. 2003. Ancient tripartite revolution in the attine ant-microbe symbiosis. Science 299:386-388.
15. Currie, C. R., M. Poulsen, J. Mendenhall, J. J. Boomsma, and J. Billen. 2006. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81-83.
16. de Fine Licht, H. H., J. J. Boomsma, and D. K. Aanen. 2007. Asymmetric interaction specificity between two sympatric termites and their fungal symbionts. Ecological Entomology 32:76-81.
17. Dentinger, B. T. M., D. J. Lodge, A. B. Munkacsi, D. E. Desjardin, and D. J. McLaughlin. 2009. Phylogenetic placement of an unusual coral mushroom challenges the classic hypothesis of strict revolution in the Apterostigma pilosum group ant-fungus mutualism. Evolution 63:2172-2178.
18. De Vienne, D. M., T. Giraud, and J. A. Shykoff. 2007. When can host shifts produce congruent host and parasite phylogenies? a simulation approach. Journal of Evolutionary Biology 20:1428-1438.
19. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
20. Dunlap, P. V., J. C. Ast, S. Kimura, A. Fukui, T. Yoshino, and H. Endo. 2007. Phylogenetic analysis of host-symbiont specificity and codivergence in bioluminescent symbioses. Ciadistics 23:507-532.
21. Fowler, H. G., and N. B. Saes. 1986. Dependence of the activity of grazing cattle on foraging grass-cutting ants Atta spp. in the southern Neotropics. Journal of Applied Entomology 101:154-158.
22. Geml, J., D. M. Geiser, and D. J. Royse. 2004. Molecular evolution of Agaricus species based on ITS and LSU rDNA sequences. Mycological Progress 3:157-176.
23. Green, A. M., U. G. Mueller, and R. M. M. Adams. 2002. Extensive exchange of fungal cultivars between sympatric species of fungusgrowing ants. Molecular Ecology 11:191-195.
24. Guimarães, P. R., V. Rico-Gray, P. S. Oliveira, T. J. Izzo, S. F. dos Reis, and J. N. Thompson. 2007. Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Current Biology 17:1797-1803.
25. Hafner, M. S., and S. A. Nadler. 1988. Phylogenetic trees support the revolution of parasites and their hosts. Nature 332:258-259.
26. Herre, E. A., K. C. Jander, and C. A. Machado. 2008. Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annual Review of Ecology, Evolution, and Systematics 39: 439-458.
27. Hinkle, G., J. K. Wetterer, T. R. Schultz, and M. L. Sogin. 1994. Phylogeny of the attine ant fungi based on analysis of small subunit ribosomal RNA gene sequences. Science 266:1695-1697.
28. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
29. Jackson, A. P., C. A. Machado, N. Robbins, and E. A. Herre. 2008. Multi-locus phylogenetic analysis of Neotropical figs does not support co-speciation with the pollinators: The importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45:57-72.
30. Jousselin, E., S. van Noort, V. Berry, J. Y. Rasplus, N. Ronsted, J. C. Erasmus, and J. M. Greeff. 2008. One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62:1777-1797. (Pubitemid 352000103)
31. Lo, N., C. Bandi, H. Watanabe, C. Nalepa, and T. Beninati. 2003. Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Molecular Biology and Evolution 20:907-913. (Pubitemid 36578717)
32. Machado, C. A., N. Robbins, M. T. P. Gilbert, and E. A. Herre. 2005. Critical review of host specificity and its coevolutionary implica-tions in the fig/fig-wasp mutualism. Proceedings of the National Academy of Sciences of the USA 102:6558-6565.
33. Mehdiabadi, N. J., B. Hughes, and U. G. Mueller. 2006. Cooperation, conflict, and coevolution in the attine ant-fungus symbiosis. Behavioral Ecology 17:291-296.
34. Memmott, J., N. M. Waser, and M. V. Price. 2004. Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B: Biological Sciences 271:2605-2611. (Pubitemid 40502595)
35. Mikheyev, A. S., U. G. Mueller, and P. Abbot. 2006. Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis. Proceedings of the National Academy of Sciences of the USA 103: 10702-10706.
36. Mikheyev, A. S., U. G. Mueller, and J. J. Boomsma. 2007. Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi. Molecular Ecology 16:209-216.
37. Mikheyev, A. S., T. Vo, and U. G. Mueller. 2008. Phylogeography of post-Pleistocene population expansion in a fungus-gardening ant and its microbial mutualists. Molecular Ecology 17:4480-4488.
38. Montoya, J. M., S. L. Pimm, and R. V. Solé. 2006. Ecological networks and their fragility. Nature 442:259-264.
39. Moran, N. A., J. P. McCutcheon, and A. Nakabachi. 2008. Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42:165-190.
40. Mueller, U. G., S. A. Rehner, and T. R. Schultz. 1998. The evolution of agriculture in ants. Science 281:2034-2038.
41. Mueller, U. G., N. M. Gerardo, D. K. Aanen, D. L. Six, and T. R. Schultz. 2005. The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics 36:563-595.
42. Munkacsi, A. B., J. J. Pan, P. Villesen, U. G. Mueller, M. Blackwell, and D. J. McLaughlin. 2004. Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants. Proceedings of the Royal Society B: Biological Sciences 271:1777-1782. (Pubitemid 40502730)
43. Noda, S., O. Kitade, T. Inoue, M. Kawai, M. Kanuka, K. Hiroshima, Y Hongoh, et al. 2007. Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Molecular Ecology 16:1257-1266.
44. Ollerton, J. 2006. "Biological barter": patterns of specialization compared across different mutualisms. Pages 411-435 in N. M. Waser and J. Ollerton, eds. Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago.
45. Page, R. D. M. 2003. Tangled trees: phylogeny, cospeciation, and coevolution. University of Chicago Press, Chicago.
46. Piercey-Normore, M. D., and P. T. DePriest. 2001. Algal switching among lichen symbioses. American Journal of Botany 88:1490-1498.
47. Quinlan, R. J., and J. M. Cherrett. 1979. The role of fungus in the diet of the leaf-cutting ant Atta cephalotes (L.). Ecological Entomology 4:151-160.
48. Rambaut, A., and A. J. Drummond. 2007. Tracer, version 1. 4. http://beast.bio.ed.ac.uk/tracer.
49. Rezende, E. L., J. E. Lavabre, P. R. Guimaraes, P. Jordano, and J. Bascompte. 2007. Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448:925-926.
50. Rikkinen, J., I. Oksanen, and K. Lohtander. 2002. Lichen guilds share related cyanobacterial symbionts. Science 297:357-357
51. Robinson, S. W., and H. G. Fowler. 1982. Foraging and pest potential of Paraguayan grass-cutting ants (Atta and Acromyrmex) to the cattle industry. Zeitschrift für Angewandte Entomologie 93:42-54.
52. Schardl, C. L., K. D. Craven, S. Speakman, A. Stromberg, A. Lindstrom, and R. Yoshida. 2008. A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Systematic Biology 57:483-498.
53. Schultz, T. R., and S. G. Brady. 2008. Major evolutionary transitions in ant agriculture. Proceedings of the National Academy of Sciences of the USA 105:5435-5440.
54. Schultz, T. R., and R. Meier. 1995. A phylogenetic analysis of the fungus-growing ants (Hymenoptera: Formicidae: Attini) based on morphological characters of the larvae. Systematic Entomology 20: 337-370.
55. Shefferson, R. P., D. L. Taylor, M. Weiss, S. Garnica, M. K. McCormick, S. Adams, H. M. Gray, et al. 2007. The evolutionary history of mycorrhizal specificity among lady's slipper orchids. Evolution 61:1380-1390.
56. Silva-Pinhati, A. C. O., M. J. Bacci Jr., G. Hinkle, M. L. Sogin, F. C. Pagnocca, V. G. Martins, O. C. Bueno, and M. J. A. Hebling. 2004. Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae). Brazilian Journal of Medical and Biological Research 37:1463-1472.
57. Smith, C. I., W K. W Godsoe, S. Tank, J. B. Yoder, and O. Pellmyr. 2008. Distinguishing coevolution from covicariance in an obligate pollination mutualism: asynchronous divergence in Joshua tree and its pollinators. Evolution 62:2676-2687.
58. Thompson, J. N. 2005. Geographic mosaic of coevolution. University of Chicago Press, Chicago.
59. Vo, T., U. G. Mueller, and A. S. Mikheyev. 2009. Free-living fungal symbionts (Lepiotaceae) of fungus-growing ants (Attini: Formicidae). Mycologia 101:206-210.
60. Weber, N. A. 1972. Gardening ants: The attines. Memoirs of the American Philosophical Society 92. American Philosophical Society, Philadelphia.
61. Wetterer, J. K., T. R. Schultz, and R. Meier. 1998. Phylogeny of fungusgrowing ants (tribe Attini) based on mtDNA sequence and morphology. Molecular Phylogenetics and Evolution 9:42-47.
62. White, T. J., T. D. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315-322 in M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White, eds. PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA.
63. Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis. University of Texas, Austin.