Evolutionary Biology

, Volume 41, Issue 1, pp 22–28 | Cite as

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

  • Pierre-Jean G. Malé
  • Jean-Baptiste Ferdy
  • Céline Leroy
  • Olivier Roux
  • Jérémie Lauth
  • Arthur Avilez
  • Alain Dejean
  • Angélique Quilichini
  • Jérôme Orivel
Research Article


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.


Evolutionary 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).

Supplementary material

11692_2013_9242_MOESM1_ESM.doc (70 kb)
Supplementary material 1 (DOC 69 kb)


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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Pierre-Jean G. Malé
    • 1
    • 2
    • 7
  • Jean-Baptiste Ferdy
    • 1
    • 2
  • Céline Leroy
    • 3
  • Olivier Roux
    • 4
  • Jérémie Lauth
    • 5
  • Arthur Avilez
    • 1
    • 2
  • Alain Dejean
    • 5
    • 6
  • Angélique Quilichini
    • 5
  • Jérôme Orivel
    • 5
  1. 1.ENFA, UMR5174 EDB (Laboratoire Évolution & Diversité Biologique)Université de ToulouseToulouseFrance
  2. 2.UMR5174 EDBCNRS, Université Paul SabatierToulouseFrance
  3. 3.UMR 123, AMAP (botAnique et bioinforMatique de l’Architecture des Plantes)IRDMontpellier Cedex 5France
  4. 4.UMR 224, Maladies Infectieuses et Vecteurs Ecologie, Génétique, Evolution et ContrôleIRDBobo Dioulasso 01Burkina Faso
  5. 5.UMR 8172, Ecologie des Forêts de GuyaneCNRSKourou CedexFrance
  6. 6.UMR EcolabUniversité de ToulouseToulouse Cedex 9France
  7. 7.Laboratoire Evolution & Diversité BiologiqueUniversité Paul SabatierToulouse Cedex 9France

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