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.
KeywordsEvolutionary conflict Cheater Overexploitation Mutualism breakdown Allomerus decemarticulatus Hirtella physophora
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).
- Bates, D., & Maechler, M. (2009). lme4: Linear mixed-effects models using S4 classes. (R package version 0.999375-32 ed.).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., 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.PubMedCentralCrossRefGoogle Scholar
- Fox, J., & Weisberg, S. (2011). An R companion to applied regression. Thousand Oaks, CA: Sage.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
- 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
- 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.PubMedCrossRefGoogle 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.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.CrossRefGoogle 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.).Google Scholar
- R Development Core Team (2009). R: A Language and Environment for Statistical Computing. In R. F. f. S. Computing (Ed.). Vienna, Austria.Google Scholar
- 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
- Zeileis, A., & Hothorn, T. (2002). Diagnostic checking in regression relationships. R News, 2(3), 7–10.Google Scholar