An evaluation of the possible adaptive function of fungal brood covering by attine ants

Evolution

Volumn 66, Issue 6, 2012, Pages 1966-1975

  Armitage, Sophie A O ^a,b   Fernández Marín, Hermógenes ^a,c   Wcislo, William T ^c   Boomsma, Jacobus J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

Formicidae; Fungus growing ants; Mycelium; Parasites; Prophylactic behavior; Pupae

Indexed keywords

ADAPTATION; ANT; ANTIBIOTICS; BROOD REARING; COCOON; COLONY; CUTICLE; EVOLUTIONARY BIOLOGY; FUNGUS; HOST-PARASITE INTERACTION; OBLIGATE BEHAVIOR; PHYLOGENETICS; RISK ASSESSMENT; SYMBIOSIS;

ADAPTATION; ANIMAL; ANIMAL BEHAVIOR; ANT; ARTICLE; FUNGUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYLOGENY; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTS; BEHAVIOR, ANIMAL; FUNGI; MICROSCOPY, ELECTRON, SCANNING; PHYLOGENY;

ATTINI; BACTERIA (MICROORGANISMS); FORMICIDAE; FUNGI; MYCELIUM (GENUS); MYRMICINAE;

EID: 84861680405     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01568.x     Document Type: Article

References (70)

1. Adams, R. M., U. G. Mueller, T. R. Schultz, and B. Norden 2000. Agro-predation: usurpation of attine fungus gardens by Megalomyrmex ants. Naturwissenschaften 87:549-554. Antweb. Available at. Accessed August 11, 2009.
2. Bacci, M. C., S. E. Solomon, U. G. Mueller, V. G. Martins, A. O. R. Carvalho, L. G. E. Vieira, and A. C. O. Silva-Pinhati 2009. Phylogeny of leafcutter ants in the genus Atta Fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences. Mol. Phylogenet. Evol. 51:427-437.
3. Barke, J., R. F. Seipke, S. Grüschow, D. Heavens, N. Drou, M. J. Bibb, R. J. M. Goss, D. W. Yu, and M. I. Hutchings 2010. A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol. 8:109-118.
4. Baroni Urbani, C., B. Bolton, and P. S. Ward 1992. The internal phylogeny of ants (Hymenoptera: Formicidae). Sys. Entomol. 17:301-329.
5. Boomsma, J. J. and D. K. Aanen 2009. Rethinking crop-disease management in fungus-growing ants. Proc. Natl. Acad. Sci. USA 106:17611-17612.
6. Boomsma, J. J., P. Schmid-Hempel, and W. O. H. Hughes 2005. Life histories and parasite pressure across the major groups of social insects. Pp. 139-175 in M. Fellowes, G. Holloway, and J. Rolff, eds. Insect evolutionary ecology. CABI, Wallingford, England
7. Brady, S. N. G., T. R. Schultz, B. L. Fisher, and P. S. Ward 2006. Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl. Acad. Sci. USA 103:18172-18177.
8. Cafaro, M. J., M. Poulsen, A. E. F. Little, S. L. Price, N. M. Gerardo, B. Wong, A. E. Stuart, B. Larget, P. Abbot, C. R. Currie 2011. Specificity in the symbiotic association between fungus growing ants and protective Pseudonocardia bacteria. Proc. R. Soc. Lond. B 278:1814-1822.
9. Camargo, R. S., L. C. Forti, J. F. S. Lopes, and A. P. P. Andrade 2006a. Brood care and male behavior in queenless Acromyrmex subterraneus brunneus (Hymenoptera: Formicidae) colonies under laboratory conditions. Sociobiology 48:717-726.
10. Camargo, R. S., J. F. S. Lopes, and L. C. Forti 2006b. Behavioural responses of workers towards worker-produced male larvae and queen-produced worker larvae in Acromyrmex subterraneus brunneus Forel, 1911 (Hym., Formicidae). J. Appl. Entomol. 130:56-60.
11. Chao, J. T., and H. R. Hermann 1983. Spinning and external ontogenetic changes in the pupae of Polistes annularis (Hymenoptera: Vespidae: Polistinae). Insectes Soc. 30:496-507.
12. Chapman, R. F. 1998. The insects: structure and function. Cambridge Univ. Press, Cambridge, U.K
13. Craig, C. L. 1997. Evolution of arthropod silks. Annu. Rev. Entomol. 42:231-267.
14. Cremer, S., S. A. O. Armitage, P. Schmid-Hempel 2007. Social Immunity. Curr. Biol. 17:R693-R702.
15. Currie, C. R., U. G. Mueller, and D. Malloch 1999. The agricultural pathology of ant fungus gardens. Proc. Natl. Acad. Sci. USA 96:7998-8002.
16. Currie, C. R., A. N. M. Bot, and J. J. Boomsma 2003. Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101:91-102.
17. 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.
18. Dijkstra, M. B., D. R. Nash, and J. J. Boomsma 2005. Self-restraint and sterility in workers of Acromyrmex and Atta leafcutter ants. Insectes Soc. 52: 67-76.
19. Do Nascimento, R. R., E. Schoeters, E. D. Morgan, J. Billen, and D. J. Stradling 1996. Chemistry of metapleural gland secretions of three attine ants, Atta sexdens rubropilosa, Atta cephalotes, and Acromyrmex octospinosus (Hymenoptera: Formicidae). J. Chem. Ecol. 22:987-1000.
20. Fernández-Marín, H., J. K. Zimmerman, and W. T. Wcislo 2006a. Acanthopria and Mimopriella parasitoid wasps (Diapriidae) attack Cyphomyrmex fungus-growing ants (Formicidae, Attini). Naturwissenschaften 93:17-21.
21. Fernández-Marín, H., J. K. Zimmerman, S. A. Rehner, and W. T. Wcislo 2006b. Active use of the metapleural glands by ants in controlling fungal infection. Proc. R. Soc. Lond. B 273:1689-1689.
22. Fernández-Marín, H., J. K. Zimmerman, D. R. Nash, J. J. Boomsma, and W. T. Wcislo 2009. Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc. R. Soc. Lond. B 276:2263-2269.
23. Freeland, W. J. 1976. Pathogens and the evolution of primate sociality. Biotropica 8:12-24.
24. Garland, T., P. H. Harvey, and A. R. Ives 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:18-18.
25. Hamilton, W. D. 1987. Kinship, recognition, disease and intelligence. Pp. 81-102 in Y. Ito, J. L. Brown, and J. Kikkawa, eds. Animal societies: theories and facts. Japan Scientific Societies Press, Tokyo
26. Hervey, A., and M. S. R. Nair 1979. Antibiotic metabolite of a fungus cultivated by gardening ants. Mycologia 71:1064-1066.
27. Hölldobler, B., and E. O. Wilson 1990, The ants. Harvard Univ. Press, Cambridge, MA
28. Hughes, W. O. H., R. Pagliarini, H. B. Madsen, M. B. Dijkstra, and J. J. Boomsma 2008. Antimicrobial defense shows an abrupt evolutionary transition in the fungus-growing ants. Evolution 62:1252-1257.
29. Ishay, J., and F. Ruttner 1971. Thermoregulation im Hornissennest. Zeitschrift für Vergleichende Physiologie 72:423-434.
30. Ishay, J. S., and E. Ganor 1990. Comb cells and puparial silk in the oriental hornet nest: Structure and function. J. Morphol. 203:11-19.
31. LaPolla, J. S., U. G. Mueller, M. Seid, and S. P. Cover 2002. Predation by the army ant Neivamyrmex rugulosus on the fungus-growing ant Trachymyrmex arizonensis. Insectes Soc. 49:251-256.
32. Little, A. E. F., and C. R. Currie 2008. Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216-1222
33. Loiácono, M. S., C. B. Margarita, M. E. Quiran, B. M. Corro Molas 2000. Diápridos (Hymenoptera) parasitoides de larvas de la hormiga cortadora Acromyrmex lobicornis (Hymenoptera: Formicidae) en la Argentina. Rev. Soc. Entomol. Argentina 59:7-15.
34. Lopes, J. F. S., W. O. H. Hughes, R. S. Camargo, and L. C. Forti 2005. Larval isolation and brood care in Acromyrmex leaf-cutting ants. Insectes Soc. 52:333-338.
35. Maddison, W. P., and D. R. Maddison 2009. Mesquite: a modular system for evolutionary analysis, version 2.6. Available at:
36. Michener, C. D. 1977. Discordant evolution and the classification of allodapine bees. Syst. Zool. 26:32-56.
37. Midford, P. E., T. Garland, and W. P. Maddison 2008. PDAP Package of Mesquite, version 2.6. Available at:
38. Moreau, C. S., C. D. Bell, R. Vila, S. B. Archibald, and N. E. Pierce 2006. Phylogeny of the ants: diversification in the age of angiosperms. Science 312:101-104.
39. Mueller, U. G. 2002. Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. Amer. Nat. 160:S67-S98.
40. Mueller, U. G., D. Dash, C. Rabeling, and A. Rodrigues 2008. Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62:2894-2912.
41. Mueller, U. G., A. Ortiz, and M. Bacci 2010. Planting of fungus onto hibernating workers of the fungus-growing ant Mycetosoritis clorindae (Attini, Formicidae). Insectes Soc. 57:209-215.
42. Nair, M., and A. Hervey 1979. Structure of lepiochlorin, an antibiotic metabolite of a fungus cultivated by ants. Phytochemistry 18:326-327.
43. Nirmala, X., D. Kodrík, M. Žurovec, and F. Sehnal 2001. Insect silk contains both a Kunitz-type and a unique Kazal-type proteinase inhibitor. Eur. J. Biochem. 268:2064-2073.
44. Oertel, E. 1930. Metamorphosis in the honeybee. J. Morphol. 50:295-339.
45. Pérez-Ortega, B., H. Fernández-Marín, M. S. Loiácono, P. Galgani, and W. T. Wcislo 2010. Biological notes on a fungus-growing ant, Trachymyrmex cf. zeteki (Hymenoptera, Formicidae, Attini) attacked by a diverse community of parasitoid wasps (Hymenoptera, Diapriidae). Insectes Soc. 57:317-322.
46. Plotkin, M., N. Y. Ermakov, S. Volynchik, D. J. Bergman, and J. S. Ishay 2007. Prevention of hyperthermia with silk of the oriental hornet, Vespa orientalis: a hypothesis. Microsc. Res. Tech. 70:69-75.
47. Poulsen, M., A. N. M. Bot, M. G. Nielsen, and J. J. Boomsma 2002. Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behav. Ecol. Sociobiol. 52:151-157.
48. Powell, S., and E. Clark 2004. Combat between large derived societies: a subterranean army ant established as a predator of mature leaf-cutting ant colonies. Insectes Soc. 51:342-351.
49. Powell, S., and N. R. Franks 2006. Ecology and the evolution of worker morphological diversity: a comparative analysis with Eciton army ants. Funct. Ecol. 20:1105-1114.
50. Rabeling, C., J. M. Brown, and M. Verhaagh 2008. Newly discovered sister lineage sheds light on early ant evolution. Proc. Natl. Acad. Sci. USA 105:14913-14917.
51. Schmid-Hempel, P. 1998. Parasites in social insects. Princeton Univ. Press, Princeton, NJ
52. Schoenian, I., M. Spiteller, M. Ghaste, R. Wirth, H. Herz, and D. Spiteller 2011. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc. Natl. Acad. Sci. USA 108:1955-1960.
53. Schultz, T. R., and S. N. G. Brady 2008. Major evolutionary transitions in ant agriculture. Proc. Natl. Acad. Sci. 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. Sys. Entomol. 20:337-370.
55. Sen, R., H. D. Ishak, D. Estrada, S. E. Dowd, E. Hong, and U. G. Mueller 2009. Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc. Natl. Acad. Sci. USA 106:17805-17810.
56. Shabtai, Y., and J. S. Ishay 1998. Hornet silk caps maintain a clean room environment: a device for filtering out bacteria and dust particles. Comp. Biochem. Physiol. A 120:565-570.
57. Shattuck, S. O. 1992. Higher classification of the ant subfamilies Aneuretinae, Dolichoderinae and Formicinae (Hymenoptera: Formicidae). Sys. Entomol. 17:199-206.
58. Sherman, P. W., T. D. Seeley, and H. K. Reeve 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131:602-610.
59. Sumner, S., D. K. Aanen, J. Delabie, and J. J. Boomsma 2004. The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery's rule. Insectes Soc. 51:37-42.
60. Tagawa, J. 1996. Function of the cocoon of the parasitoid wasp, Cotesia glomerata L. (Hymenoptera: Braconidae): protection against desiccation. App. Entomol. Zool. 31:99-103.
61. Taylor, R. W. 2007. Bloody funny wasps! Speculations on the evolution of eusociality in ants. Pp. 580-609 in R. R. Snelling, B. L. Fisher, and P. S. Ward, eds. Advances in ant systematics (Hymenoptera: Formicidae): homage to E. O. Wilson - 50 years of contributions, Memoirs of the American Entomological Institute, Gainesville, FL.
62. Van Bael, S. A., H. Fernandez-Marin, M. C. Valencia, E. I. Rojas, W. T. Wcislo, and E. A. Herre 2009. Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. Proc. R. Soc. Lond. B 276:2419-2419.
63. van Noordwijk, A. J., and G. de Jong 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128:137-142.
64. Villesen, P., T. Murakami, T. R. Schultz, and J. J. Boomsma 2002. Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. B 269:1541-1548
65. Wang, Y., U. G. Mueller, and J. O. N. Clardy 1999. Antifungal diketopiperazines from symbiotic fungus of fungus-growing ant Cyphomyrmex minutus. J. Chem. Ecol. 25:935-941.
66. Weber, N. A. 1972. Gardening ants: the attines. Mem. Am. Phil. Soc. 92:1-146.
67. Wheeler, G. C. 1948. The larvae of the fungus-growing ants. Amer. Mid. Nat. 40:664-689.
68. Wheeler, W. M. 1907. The fungus-growing ants of North America. Bull. Amer. Mus. Nat. Hist. 23:669-807.
69. Wheeler, W. M. 1915. On the presence and absence of cocoons among ants, the nest-spinning habits of the larvae and the significance of the black cocoons among certain Australian species. Ann. Entomol. Soc. Amer. 8:323-342.
70. Yek, A. H., and U. G. Mueller 2011. The metapleural gland of ants. Biol. Rev. 86:774-791.