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Retaliation in Response to Castration Promotes a Low Level of Virulence in an Ant–Plant Mutualism


The diversion of a host’s energy by a symbiont for its own benefit is a major source of instability in horizontally-transmitted mutualisms. This instability can be counter-balanced by the host’s retaliation against exploiters. Such responses are crucial to the maintenance of the relationship. We focus on this issue in an obligate ant–plant mutualism in which the ants are known to partially castrate their host plant. We studied plant responses to various levels of castration in terms of (1) global vegetative investment and (2) investment in myrmecophytic traits. Castration led to a higher plant growth rate, signalling a novel case of gigantism induced by parasitic castration. On the other hand, completely castrated plants produced smaller nesting and food resources (i.e. leaf pouches and extra floral nectaries). Since the number of worker larvae is correlated to the volume of the leaf pouches, such a decrease in the investment in myrmecophytic traits demonstrates for the first time the existence of inducible retaliation mechanisms against too virulent castrating ants. Over time, this mechanism promotes an intermediate level of castration and enhances the stability of the mutualistic relationship by providing the ants with more living space while allowing the plant to reproduce.

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  • Bates, D., & Maechler, M. (2009). lme4: Linear mixed-effects models using S4 classes. (R package version 0.999375-32 ed.).

  • Best, A., White, A., & Boots, M. (2009). Resistance is futile but tolerance can explain why parasites do not always castrate their hosts. Evolution, 64(2), 348–357. doi:10.1111/j.1558-5646.2009.00819.x.

    PubMed  Article  Google Scholar 

  • Bronstein, J. L. (2001). The exploitation of mutualisms. Ecology Letters, 4(3), 277–287.

    Article  Google Scholar 

  • Douglas, A. E. (2008). Conflict, cheats and the persistence of symbioses. New Phytologist, 177(4), 849–858. doi:10.1111/j.1469-8137.2007.02326.x.

    PubMed  Article  Google Scholar 

  • Douglas, A. E. (2010). The symbiotic habit. Princeton and Oxford: Princeton University Press.

    Google Scholar 

  • Dussutour, A., & Simpson, S. J. (2012). Ant workers die young and colonies collapse when fed a high-protein diet. In Proceedings of the Royal Society B-Biological Sciences: online. doi:10.1098/rspb.2012.0051.

  • Edwards, D. P., Ansell, F. A., Woodcock, P., Fayle, T. M., Chey, V. K., & Hamer, K. C. (2010). Can the failure to punish promote cheating in mutualism? Oikos, 119, 45–52. doi:10.1111/j.1600-0706.2009.17591.x.

    Article  Google Scholar 

  • Edwards, D. P., Hassall, M., Sutherland, W. J., & Yu, D. W. (2006). Selection for protection in an ant–plant mutualism: host sanctions, host modularity, and the principal–agent game. Proceedings of the Royal Society B-Biological Sciences, 273, 595–602. doi:10.1098/rspb.2005.3273.

    PubMed Central  Article  Google Scholar 

  • Edwards, D. P., & Yu, D. W. (2008). Tolerating castration by hiding flowers in plain sight. Behavioral Ecology and Sociobiology, 63(1), 95–102. doi:10.1007/s00265-008-0639-8.

    Article  Google Scholar 

  • Fonseca, C. R. (1993). Nesting space limits colony size of the plant–ant Pseudomyrmex concolor. Oikos, 67, 473–482.

    Article  Google Scholar 

  • Fox, J., & Weisberg, S. (2011). An R companion to applied regression. Thousand Oaks, CA: Sage.

    Google Scholar 

  • Frederickson, M. E. (2009). Conflict over reproduction in an ant-plant symbiosis: Why Allomerus octoarticulatus ants sterilize Cordia nodosa trees? American Naturalist, 173(5), 675–681. doi:10.1086/597608.

    PubMed  Article  Google Scholar 

  • Gaume, L., Zacharias, M., & Borges, R. M. (2005). Ant–plant conflicts and a novel case of castration parasitism in a myrmecophyte. Evolutionary Ecology Research, 7, 435–452.

    Google Scholar 

  • Gilbert, F. S., Haines, N., & Dickson, K. (1991). Empty flowers. Functional Ecology, 5, 29–39.

    Article  Google Scholar 

  • Grangier, J., Dejean, A., Malé, P.-J. G., & Orivel, J. (2008). Indirect defense in a highly specific ant–plant mutualism. Naturwissenschaften, 95(10), 909–916. doi:10.1007/s00114-008-0398-4.

    CAS  PubMed  Article  Google Scholar 

  • Grangier, J., Dejean, A., Malé, P.-J. G., Solano, P.-J., & Orivel, J. (2009). Mechanisms driving the specificity of a myrmecophyte–ant association. Biological Journal of the Linnean Society, 97, 90–97. doi:10.1111/j.1095-8312.2008.01188.x.

    Article  Google Scholar 

  • Hall, S. R., Becker, C., & Cáceres, C. E. (2007). Parasitic castration: A perspective from a model of dynamic energy budgets. Integrative and Comparative Biology, 47(2), 295–309. doi:10.1093/icb/icm057.

    PubMed  Article  Google Scholar 

  • Heil, M., & McKey, D. (2003). Protective ant–plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology Evolution and Systematics, 34, 425–453.

    Article  Google Scholar 

  • Herre, E. A., Knowlton, N., Mueller, U. G., & Rehner, S. A. (1999). The evolution of mutualisms: Exploring the paths between conflict and cooperation. Trends in Ecology & Evolution, 14(2), 49–53. doi:10.1016/S0169-5347(98)01529-8.

    Article  Google Scholar 

  • Inouye, D. W. (1983). The ecology of nectar robbing. In B. Bentley & T. Elias (Eds.), The biology of nectaries. New York, USA: Columbia University Press.

    Google Scholar 

  • Izzo, T. J., & Vasconcelos, H. L. (2002). Cheating the cheater: Domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia, 133, 200–205. doi:10.1007/s00442-002-1027-0.

    Article  Google Scholar 

  • Jaenike, J. (1996). Suboptimal virulence of an insect–parasitic nematode. Evolution, 50(6), 2241–2247.

    Article  Google Scholar 

  • Leroy, C., Jauneau, A., Quilichini, A., Dejean, A., & Orivel, J. (2008). Comparison between the anatomical and morphological structure of leaf blades and foliar domatia in the ant–plant Hirtella physophora (Chrysobalanaceae). Annals of Botany, 101, 501–507. doi:10.1093/aob/mcm323.

    PubMed  Article  Google Scholar 

  • Leroy, C., Jauneau, A., Quilichini, A., Dejean, A., & Orivel, J. (2010). Comparative structure and ontogeny of the foliar domatia in three neotropical myrmecophytes. American Journal of Botany, 97, 557–565. doi:10.3732/ajb.0900207.

    PubMed  Article  Google Scholar 

  • Malé, P.-J. G. (2011). Stabilité évolutive des mutualismes et mécanismes de contrôle : le cas d’une relation plante-fourmis. PhD thesis, Université de Toulouse, Toulouse, France.

  • Malé, P.-J. G., Leroy, C., Dejean, A., Quilichini, A., & Orivel, J. (2012). An ant symbiont directly and indirectly limits its host plant’s reproductive success. Evolutionary Ecology, 26(1), 55–63. doi:10.1007/s10682-011-9485-7.

    Article  Google Scholar 

  • Obeso, J. R. (2002). The cost of reproduction in plants. New Phytologist, 155, 321–348. doi:10.1046/j.1469-8137.2002.00477.x.

    Article  Google Scholar 

  • O’Keefe, K. J., & Antonovics, J. (2002). Playing by different rules: The evolution of virulence in sterilizing pathogens. American Naturalist, 159(6), 597–605. doi:10.1086/339990.

    PubMed  Article  Google Scholar 

  • Orivel, J., Lambs, L., Malé, P.-J. G., Leroy, C., Grangier, J., Otto, T., et al. (2011). Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants. Oecologia, 165, 369–376. doi:10.1007/s00442-010-1739-5.

    PubMed  Article  Google Scholar 

  • Pacini, E., Nepi, M., & Vesprini, J. L. (2003). Nectar biodiversity: A short review. Plant Systematics and Evolution, 238, 7–21. doi:10.1007/s00606-002-0277-yNectar.

    CAS  Google Scholar 

  • Palmer, T. M., Doak, D. F., Stanton, M. L., Bronstein, J. L., Kiers, E. T., Young, T. P., et al. (2010). Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proceedings of the National Academy of Sciences, 107(40), 17234–17239.

    CAS  Article  Google Scholar 

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & The R Core Team. (2009). nlme: Linear and Nonlinear Mixed Effects Models. (R package version 3.1-96 ed.).

  • R Development Core Team (2009). R: A Language and Environment for Statistical Computing. In R. F. f. S. Computing (Ed.). Vienna, Austria.

  • Solano, P.-J., Durou, S., Corbara, B., Quilichini, A., Cerdan, P., Belin-Dupoux, M., et al. (2003). Myrmecophytes of the understory of French Guianian rainforests: Their distribution and their associated ants. Sociobiology, 41(3), 605–614.

    Google Scholar 

  • Szilágyi, A., Scheuring, I., Edwards, D. P., Orivel, J., & Yu, D. W. (2009). The evolution of intermediate castration virulence and ant coexistence in a spatially structured environment. Ecology Letters, 12(12), 1306–1316.

    PubMed  Article  Google Scholar 

  • Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York: Springer.

    Book  Google Scholar 

  • Watson, M. A. (1984). Developmental constraints: effect on population growth and patterns of resource allocation in a clonal plant. American Naturalist, 123(3), 411–426. doi:10.1086/284212.

    Article  Google Scholar 

  • West, S. A., Kiers, E. T., Simms, E. L., & Denison, R. F. (2002). Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proceedings of the Royal Society B-Biological Sciences, 269, 685–694. doi:10.1098/rspb.2001.1878.

    PubMed Central  Article  Google Scholar 

  • Wilkinson, D. M., & Sherratt, T. N. (2001). Horizontally acquired mutualisms, an unsolved problem in ecology? Oikos, 92(2), 377–384. doi:10.1034/j.1600-0706.2001.920222.x.

    Article  Google Scholar 

  • Yu, D. W., & Pierce, N. E. (1998). A castration parasite of an ant-plant mutualism. Proceedings of the Royal Society B-Biological Sciences, 265, 375–382. doi:10.1098/rspb.1998.0305.

    PubMed Central  Article  Google Scholar 

  • Zeileis, A., & Hothorn, T. (2002). Diagnostic checking in regression relationships. R News, 2(3), 7–10.

    Google Scholar 

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We are grateful to the Laboratoire Environnement de Petit Saut and the Nouragues scientific station for furnishing logistical help, to Dr. Jacqui Shykoff and Pr. Doyle McKey for insightful comments and to Andrea Yockey-Dejean for proofreading the manuscript. Financial support for this study was provided by a research program of the French Agence Nationale de la Recherche (research agreement n°ANR-06-JCJC-0109-01), by the ESF-EUROCORES/TECT/BIOCONTRACT program, by the Fondation pour la Recherche sur la Biodiversité (research agreement n°AAP-IN-2009-050), by the Programme Convergence 2007–2013 Région Guyane from the European Community, and by the Programme Amazonie II of the French Centre National de la Recherche Scientifique. This work has benefited from “Investissement d’Avenir” grants managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01 and TULIP, ref. ANR -10-LABX-0041).

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Correspondence to Pierre-Jean G. Malé.

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Malé, PJ.G., Ferdy, JB., Leroy, C. et al. Retaliation in Response to Castration Promotes a Low Level of Virulence in an Ant–Plant Mutualism. Evol Biol 41, 22–28 (2014).

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  • Evolutionary conflict
  • Cheater
  • Overexploitation
  • Mutualism breakdown
  • Allomerus decemarticulatus
  • Hirtella physophora