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

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Abstract

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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Acknowledgments

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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Authors and Affiliations

  1. ENFA, UMR5174 EDB (Laboratoire Évolution & Diversité Biologique), Université de Toulouse, 118 route de Narbonne, 31062, Toulouse, France

    Pierre-Jean G. Malé, Jean-Baptiste Ferdy & Arthur Avilez

  2. UMR5174 EDB, CNRS, Université Paul Sabatier, 31062, Toulouse, France

    Pierre-Jean G. Malé, Jean-Baptiste Ferdy & Arthur Avilez

  3. UMR 123, AMAP (botAnique et bioinforMatique de l’Architecture des Plantes), IRD, Boulevard de la Lironde, TA A51/PS2, 34398, Montpellier Cedex 5, France

    Céline Leroy

  4. UMR 224, Maladies Infectieuses et Vecteurs Ecologie, Génétique, Evolution et Contrôle, IRD, BP 171, Bobo Dioulasso 01, Burkina Faso

    Olivier Roux

  5. UMR 8172, Ecologie des Forêts de Guyane, CNRS, Campus Agronomique, BP 316, 97379, Kourou Cedex, France

    Jérémie Lauth, Alain Dejean, Angélique Quilichini & Jérôme Orivel

  6. UMR Ecolab, Université de Toulouse, 118 route de Narbonne, 31062, Toulouse Cedex 9, France

    Alain Dejean

  7. Laboratoire Evolution & Diversité Biologique, Université Paul Sabatier, 118 route de Narbonne, 31062, Toulouse Cedex 9, France

    Pierre-Jean G. Malé

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  1. Pierre-Jean G. Malé
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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). https://doi.org/10.1007/s11692-013-9242-7

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  • DOI: https://doi.org/10.1007/s11692-013-9242-7

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