Abstract
Parasites represent one of the main threats to all organisms and are likely to be particularly significant for social animals because of the increased potential for intragroup transmission. Social animals must therefore have effective resistance mechanisms against parasites and one of the most important components of disease resistance in ants is thought to be the antibiotic-producing metapleural gland. This gland is ancestral in ants, but has been lost secondarily in a small number of species. It is unknown whether these evolutionary losses are due to a reduction in parasite pressure or the replacement of the gland’s function with other resistance mechanisms. Here we used the generalist entomopathogenic fungus Metarhizium to compare the disease resistance of a species of a weaver ant, Polyrhachis dives, which has lost the metapleural gland, with that of the well-studied leaf-cutting ant Acromyrmex echinatior and two other ant species, Myrmica ruginodis and Formica fusca, all of which have metapleural glands. The P. dives weaver ants had intermediate resistance when kept individually, and similar resistance to A. echinatior leaf-cutting ants when kept in groups, suggesting that the loss of the metapleural gland has not resulted in weaver ants having reduced disease resistance. P. dives weaver ants self-groomed at a significantly higher rate than the other ants examined and apparently use their venom for resistance, as they had reduced resistance when their venom gland was blocked and the venom was shown in vitro to prevent the germination of fungal spores. Unexpectedly, the leaf-cutting ant A. echinatior also had reduced resistance to Metarhizium when its venom gland was blocked. It therefore appears that the evolutionary loss of the metapleural gland does not result in reduced disease resistance in P. dives weaver ants, and that this at least in part may be due to the ants having antimicrobial venom and high self-grooming rates. The results therefore emphasise the importance of multiple, complementary mechanisms in the disease resistance of ant societies.
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References
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:324–383
Angus CJ, Jones MK, Beattie AJ (1993) A possible explanation for size differences in the metapleural glands of ants (Hymenoptera, Formicidae). J Aust Entomol Soc 32:73–77
Baer B, Krug A, Boomsma JJ, Hughes WOH (2005) Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection. Insectes Soc 52:298–303
Beattie AJ, Turnbull CL, Hough T, Knox RB (1986) Antibiotic production - a possible function for the metapleural glands of ants (Hymenoptera, Formicidae). Ann Entomol Soc Am 79:448–450
Blum MS (1992) Ant venoms: chemical and pharmacological properties. Toxin Rev 11:115–164
Bocher A, Tirard C, Doums C (2007) Phenotypic plasticity of immune defence linked with foraging activity in the ant Cataglyphis velox. J Evol Biol 20:2228–2234
Bolton B (1995) A new general catalogue of the ants of the world. Harvard University, Cambridge
Boomsma JJ, Schmid-Hempel P, Hughes WOH (2005) Life histories and parasite pressure across the major groups of social insects. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI, Wallingford, pp 139–175
Bot ANM, Boomsma JJ (1996) Variable metapleural gland size-allometries in Acromyrmex leafcutter ants (Hymenoptera: Formicidae). J Kansas Entomol Soc 69:375–383
Bot ANM, Obermayer ML, Holldobler B, Boomsma JJ (2001) Functional morphology of the metapleural gland in the leaf-cutting ant Acromyrmex octospinosus. Insectes Soc 48:63–66
Bot ANM, Ortius-Lechner D, Finster K, Maile R, Boomsma JJ (2002) Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc 49:363–370
Brown WL (1968) An hypothesis concerning function of metapleural glands in ants. Am Nat 102:188–191
Castella G, Chapuisat M, Christe P (2008) Prophylaxis with resin in wood ants. Anim Behav 75:1591–1596
De Souza ALB, Soares IMF, Cyrino LT, Serrao JE (2006) The metapleural gland of two subspecies of Acromyrmex subterraneus (Hymenoptera: Formicidae). Sociobiology 47:19–25
Fernandez-Marin H, Zimmerman J, Rehner S, Wcislo W (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc Lond B 273:1689–1695
Fountain T, Hughes WOH (2011) Weaving resistance: silk and disease resistance in the weaver ant Polyrhachis dives. Insectes Soc. doi:10.1007/s00040-011-0162-1
Hamilton WD (1987) Kinship, recognition, disease, and intelligence: constraints of social evolution. In: Ito Y, Brown JL, Kirkkawa J (eds) Animal societies: Theories and facts. Japan Scientific Societies, Tokyo, pp 81–100
Hart AG, Ratnieks FLW (2001) Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behav Ecol Sociobiol 49:387–392
Hölldobler B, Engel-Siegel H (1984) On the metapleural gland of ants. Psyche 91:201–224
Hölldobler B, Wilson EO (1990) The ants. Belknap, Cambridge
Hughes WOH, Boomsma JJ (2004) Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proc R Soc Lond B 271:S104–S106
Hughes WOH, Boomsma JJ (2006) Does genetic diversity hinder parasite evolution in social insect colonies? J Evol Biol 19:132–143
Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B 269:1811–1819
Hughes WOH, Petersen K, Ugelvig L, Pedersen D, Thomsen L, Poulsen M, Boomsma JJ (2004a) Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evol Biol 4:45
Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ (2004b) Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertbr Pathol 85:46–53
Hughes WOH, Pagliarini R, Madsen HB, Dijkstra MJ, Boomsma JJ (2008) Antimicrobial defence shows an abrupt evolutionary transition in the fungus-growing ants. Evolution 1252–1257
Hughes WOH, Bot ANM, Boomsma JJ (2010) Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants. Proc R Soc Lond B 277:609–615
Johnson RN, Agapow PM, Crozier RH (2003) A tree island approach to inferring phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving. Mol Phylogenet Evol 29:317–330
Kraus J, Ruxton GD (2002) Living in groups. Oxford University, Oxford
Lacey LA (1997) Manual of techniques in insect pathology. Academic, London
Mackintosh JA, Trimble JE, Jones MK, Karuso PH, Beattie AJ, Veal DA (1995) Antimicrobial mode of action of secretions from the metapleural gland of Myrmecia gulosa (Australian bull ants). Can J Microbiol 41:136–144
Mackintosh JA, Flood JA, Veal DA, Beattie AJ (1999) Increase in levels of microbiota recoverable from male and larval Myrmecia gulosa (Fabricius) (Hymenoptera: Formicidae) following segregation from worker ants. Aust J Entomol 38:124–126
Orivel J, Redeker V, Caer J, Krieri F, Revol-Junelles AM, Longeon A, Chaffotte A, Dejean A, Rossier J (2001) Ponericins, new antibacterial and insecticidal peptides from the venom of the ant Pachycondyla goeldii. J Biol Chem 276
Poulsen M, Bot ANM, Nielsen MG, Boomsma JJ (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
Poulsen M, Hughes WOH, Boomsma JJ (2006) Differential resistance and the importance of antibiotic production in Acromyrmex echinatior leaf-cutting ant castes towards the entomopathogenic fungus Aspergillus nomius. Insectes Soc 53:349–355
Robson SKA, Kohout RJ (2005) Evolution of nest-weaving behaviour in arboreal nesting ants of the genus Polyrhachis Fr. Smith (Hymenoptera: Formicidae). Aust J Entomol 44:164–169
Robson SKA, Kohout RJ (2007) A review of the nesting habits and socioecology of the ant genus Polyrhachis Fr. Smith. Asian Myrmecol 1:81–99
Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125–134
Rosengaus RB, Jordan C, Lefebvre ML, Traniello JFA (1999a) Pathogen alarm behavior in a termite: A new form of communication in social insects. Naturwissenschaften 86:544–548
Rosengaus RB, Traniello JFA, Chen T, Brown JJ, Karp RD (1999b) Immunity in a social insect. Naturwissenschaften 86:588–591
Rosengaus RB, Lefebvre ML, Traniello JFA (2000) Inhibition of fungal spore germination by Nasutitermes: evidence for a possible antiseptic role of soldier defensive secretions. J Chem Ecol 26:21–39
Schlüns H, Crozier RH (2009) Molecular and chemical immune defenses in ants (Hymenoptera: Formicidae). Myrmecol News 12:237–249
Schmid-Hempel P (1998) Parasites in social insects. Princeton University, Princeton
Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602–610
Storey GK, Vander Meer RK, Boucias DG, McCoy CW (1991) Effect of fire ant (Solenopsis invicta) venom alkaloids on the in vitro germination and development of selected entomogenous fungi. J Invertebr Pathol 58:88–95
Sumner S, Hughes WOH, Boomsma JJ (2003) Evidence for differential selection and potential adaptive evolution in the worker caste of an inquiline social parasite. Behav Ecol Sociobiol 54:256–263
Traniello JFA, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. PNAS 99:6838–6842
Ugelvig LV, Cremer S (2007) Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 17:1967–1971
Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc Lond B 277:2821–2828
Veal DA, Trimble JE, Beattie AJ (1992) Antimicrobial properties of secretions from the metapleural glands of Myrmecia gulosa (the Australian bull ant). J Appl Bacteriol 72:188–194
Waddington SJ, Hughes WOH (2010) Waste management in the leaf-cutting ant Acromyrmex echinatior: the role of worker size, age and plasticity. Behav Ecol Sociobiol 64(8):1219–1228. doi:10.1007/s00265-010-0936-x
Walker TN, Hughes WOH (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448
Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649
Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143
Yanagawa A, Yokohari F, Shimizu S (2008) Defense mechanism of the termite, Coptotermes formosanus Shiraki, to entomopathogenic fungi. J Invertebr Pathol 97:165–170
Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev. doi:10.1111/j.1469-185X.2010.00170.x
Zelezetsky I, Pag U, Antcheva N, Sahl HG, Tossi A (2005) Identification and optimization of an antimicrobial peptide from the ant venom toxin pilosulin. Arch Biochem Biophys 434:358–364
Acknowledgements
We are grateful to Allen Herre and the Smithsonian Tropical Research Institute for the facilities in Gamboa, the Autoridad Nacional del Ambiente (ANAM) for permission to collect and export the Acromyrmex colonies, and Martin Sebesta for providing the other ant colonies. We also thank Crystal Frost, Katherine Roberts, Lorenzo Santorelli, Toby Fountain, Sophie Evison and Adam Smith for technical assistance and discussions, the three anonymous reviewers for their comments on the manuscript and the Leverhulme Foundation for funding.
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Graystock, P., Hughes, W.O.H. Disease resistance in a weaver ant, Polyrhachis dives, and the role of antibiotic-producing glands. Behav Ecol Sociobiol 65, 2319–2327 (2011). https://doi.org/10.1007/s00265-011-1242-y
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DOI: https://doi.org/10.1007/s00265-011-1242-y