1887

Abstract

Leaf-cutting ants (genera and ) cultivate a specialized fungus for food in underground chambers employing cut plant material as substrate. Parasitism occurs in this agricultural system and plays an important role in colony fitness. The microfungi , a specialized mycoparasite of the fungal cultivar, is highly prevalent among colonies. In this study, we tested the antagonistic activity of several strains from different geographical areas in Costa Rica. We employed a combination of laboratory tests to evaluate virulence, including pure culture challenges, toxicity to fungus garden pieces and subcolony bioassays. We also performed a phylogenetic analysis of these strains in order to correlate their virulence with the genetic structure of this population. The bioassays yielded results consistent between each other and showed significant differences in antagonistic activity among the parasites evaluated. However, no significant differences were found when comparing the results of the bioassays according to the source of the ants’ fungal cultivar. The phylogenetic analyses were consistent with these results: whilst the fungal cultivar phylogeny showed a single clade with limited molecular variation, the phylogeny yielded several clades with the most virulent isolates grouping in the same well-supported clade. These results indicate that there are strains better suited to establish their antagonistic effect, whilst the genetic homogeneity of the fungal cultivars limits their ability to modulate antagonism. These findings should be taken into consideration when evaluating the potential of isolates as biocontrol agents for this important agricultural pest in the Neotropics.

Funding
This study was supported by the:
  • , Vicerrectoría de Investigación, Universidad de Costa Ric , (Award VI 810-B0-501)
  • , Fondo de Reinserción del Ministerio de Ciencia y Tecnología (MICIT)
  • , Premio Aportes a la Creatividad y la Excelencia de Florida Ice and Farm Company
  • , National Science Foundation , (Award MCB-0702025)
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2014-08-01
2021-01-18
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990). Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  2. Bender W., Spierer P., Hogness D. S., Chambon P. ( 1983). Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol 168:17–33 [CrossRef][PubMed]
    [Google Scholar]
  3. Chapela I. H., Rehner S. A., Schultz T. R., Mueller U. G. ( 1994). Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694 [CrossRef][PubMed]
    [Google Scholar]
  4. Cherrett J. M. ( 1968). Some aspects of the distribution of pest species of leaf cutting ants in the Caribbean. J Am Soc Hortic Sci 12:295–310
    [Google Scholar]
  5. Cherrett J. M. ( 1986). The biology, pest status and control of leaf cutting ants. Agric Zool Rev 1:1–27
    [Google Scholar]
  6. Currie C. R. ( 2001a). A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380 [CrossRef][PubMed]
    [Google Scholar]
  7. Currie C. R. ( 2001b). Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128:99–106 [CrossRef]
    [Google Scholar]
  8. Currie C. R., Stuart A. E. ( 2001). Weeding and grooming of pathogens in agriculture by ants. Proc Biol Sci 268:1033–1039 [CrossRef][PubMed]
    [Google Scholar]
  9. Currie C. R., Mueller U. G., Malloch D. ( 1999a). The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci U S A 96:7998–8002 [CrossRef][PubMed]
    [Google Scholar]
  10. Currie C. R., Scott J. A., Summerbell R. C., Malloch D. ( 1999b). Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704 [CrossRef]
    [Google Scholar]
  11. Currie C. R., Wong B., Stuart A. E., Schultz T. R., Rehner S. A., Mueller U. G., Sung G. H., Spatafora J. W., Straus N. A. ( 2003). Ancient tripartite coevolution in the attine ant–microbe symbiosis. Science 299:386–388 [CrossRef][PubMed]
    [Google Scholar]
  12. Gerardo N. M., Mueller U. G., Price S. L., Currie C. R. ( 2004). Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ant symbiosis. Proc Biol Sci 271:1791–1798 [CrossRef][PubMed]
    [Google Scholar]
  13. Gerardo N. M., Jacobs S. R., Currie C. R., Mueller U. G. ( 2006a). Ancient host–pathogen associations maintained by specificity of chemotaxis and antibiosis. PLoS Biol 4:e235 [CrossRef][PubMed]
    [Google Scholar]
  14. Gerardo N. M., Mueller U. G., Currie C. R. ( 2006b). Complex host–pathogen coevolution in the Apterostigma fungus-growing ant–microbe symbiosis. BMC Evol Biol 6:88–96 [CrossRef][PubMed]
    [Google Scholar]
  15. Höldobler B., Wilson E. O. ( 1990). The Ants Cambridge, MA: Harvard University Press; [CrossRef]
    [Google Scholar]
  16. Lively C. M. ( 1999). Migration, virulence, and the geographic mosaic of adaptations by parasites. Am Nat 153:S5S34–S47 [CrossRef]
    [Google Scholar]
  17. Longino J. T. ( 2004). Ants of Costa Rica. The Evergreen State College; Olympia, WA, USA: http://academic.evergreen.edu/projects/ants/genusguide/attini.html
  18. Möller A. F. ( 1893). Die Pilzgärten einiger südamerikanischer Ameisen. Jena: Gustav Fischer (in German);
  19. Mueller U. G., Rehner S. A., Schultz T. R. ( 1998). The evolution of agriculture in ants. Science 281:2034–2038 [CrossRef][PubMed]
    [Google Scholar]
  20. Penn O., Privman E., Ashkenazy H., Landan G., Graur D., Pupko T. ( 2010). guidance: a web server for assessing alignment confidence scores. Nucleic Acids Res 38:Suppl.W23–W28 [CrossRef][PubMed]
    [Google Scholar]
  21. Pinto-Tomás A. A., Anderson M. A., Suen G., Stevenson D. M., Chu F. S., Cleland W. W., Weimer P. J., Currie C. R. ( 2009). Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123 [CrossRef][PubMed]
    [Google Scholar]
  22. Posada D. ( 2008). jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 [CrossRef][PubMed]
    [Google Scholar]
  23. Poulsen M., Fernández-Marín H., Currie C. R., Boomsma J. J. ( 2009). Ephemeral windows of opportunity for horizontal transmission of fungal symbionts in leaf-cutting ants. Evolution 63:2235–2247 [CrossRef][PubMed]
    [Google Scholar]
  24. Reynolds H. T., Currie C. R. ( 2004). Pathogenicity of Escovopsis weberi: the parasite of the attine ant–microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96:955–959 [CrossRef][PubMed]
    [Google Scholar]
  25. Ronquist F., Huelsenbeck J. P. ( 2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [CrossRef][PubMed]
    [Google Scholar]
  26. Schultz T. R., Brady S. G. ( 2008). Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci U S A 105:5435–5440 [CrossRef][PubMed]
    [Google Scholar]
  27. Silva A., Rodrigues A., Bacci M. Jr, Pagnocca F. C., Bueno O. C. ( 2006). Susceptibility of the ant-cultivated fungus Leucoagaricus gongylophorus (Agaricales: Basidiomycota) towards microfungi. Mycopathologia 162:115–119 [CrossRef][PubMed]
    [Google Scholar]
  28. Stahel G. ( 1943). The fungus gardens of the leaf-cutting ants. J New York Bot Gard 44:245–253
    [Google Scholar]
  29. Suen G., Scott J. J., Aylward F. O., Adams S. M., Tringe S. G., Pinto-Tomás A. A., Foster C. E., Pauly M., Weimer P. J. & other authors ( 2010). An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet 6:e1001129 [CrossRef][PubMed]
    [Google Scholar]
  30. Taerum S. J., Cafaro M. J., Little A. E., Schultz T. R., Currie C. R. ( 2007). Low host–pathogen specificity in the leaf-cutting ant–microbe symbiosis. Proc Biol Sci 274:1971–1978 [CrossRef][PubMed]
    [Google Scholar]
  31. Taerum S. J., Cafaro M. J., Currie C. R. ( 2010). Presence of multiparasite infections within individual colonies of leaf-cutter ants. Environ Entomol 39:105–113 [CrossRef][PubMed]
    [Google Scholar]
  32. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. ( 2011). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  33. Urbas P., Araújo M. V., Leal I. R., Wirth R. ( 2007). Cutting more from cut forests: edge effects on foraging and herbivory of leaf-cutting ants in Brazil. Biotropica 39:489–495 [CrossRef]
    [Google Scholar]
  34. Varon E. H. ( 2006). Distribution and foraging by the leaf-cutting ant, Atta cephalotes L., in coffee plantations with different types of management and landscape contexts, and alternatives to insecticides for its control Dissertation: Centro Agronómico Tropical de Investigación y Enseñanza, Costa Rica;
    [Google Scholar]
  35. Weber N. A. ( 1966). Fungus-growing ants. Science 153:587–604 [CrossRef][PubMed]
    [Google Scholar]
  36. Weber N. A. ( 1972). Gardening Ants: the Attines Philadelphia, PA: American Philosophical Society;
    [Google Scholar]
  37. Weber N. A. ( 1979). Fungus culturing by ants. Insect–Fungus Symbiosis, Mutualism and Commensalisms77–116 Batra L. R. New York, NY: John Wiley;
    [Google Scholar]
  38. Wilson E. O. ( 1971). The Insect Societies Cambridge, MA: The Belknap Press of Harvard University Press;
    [Google Scholar]
  39. Wilson E. O. ( 1980). Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Behav Ecol Sociobiol 7:143–156 [CrossRef]
    [Google Scholar]
  40. Wirth R., Beyschlag W., Ryel R., Herz H., Hölldobler B. ( 2003). The herbivory of leaf-cutting ants. A case study on Atta colombica in the tropical rainforest of Panama. Ecol Studies 42:113–116
    [Google Scholar]
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