Skip to main content
SpringerLink
Log in

The Evolution of Communication in Two Ant-Plant Mutualisms

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Myrmecophytes are plants that provide nesting sites and food to ants that protect them against herbivores. Plant signals function to synchronize ant patrolling with the probability of herbivory. We compared the communication signals in two symbioses involving ant and plant pairs that are closely related. The two plants emitted the same volatile compounds upon damage. These compounds are simple molecules common in the plant kingdom. Electroantennography revealed that the two symbiotic ants, as well as several other ant species, were able to perceive these compounds. However, workers of one species responded only to hexanal, while those of the other species responded mostly to methyl salicylate. The two signals involved in the focal symbioses are ‘cheap’ (low metabolic cost), which is consistent with theoretical predictions for the evolution of signalling between partners with convergent interests. They are also not specific, which is expected between plants and broad-spectrum predators such as ants. The fact that different signals are used in the two sister symbioses suggests different mechanisms underlying similar adaptations in the evolution of communication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectroscopy. Carol Stream, IL, USA: Allured Publishing.

    Google Scholar 

  • Arimura, G., Matsui, K., & Takabayashi, J. (2009). Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions. Plant and Cell Physiology, 50(5), 911–923.

    Article  PubMed  CAS  Google Scholar 

  • Becerra, J. X., Noge, K., & Venable, D. L. (2009). Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proceedings of the National Academy of Sciences of the United States of America, 106(43), 18062–18066.

    Article  PubMed  CAS  Google Scholar 

  • Blatrix, R., & Mayer, V. (2010). Communication in ant-plant symbioses. In F. Baluska & V. Ninkovic (Eds.), Plant communication from an ecological perspective (pp. 127–158). Berlin: Springer.

    Chapter  Google Scholar 

  • Brouat, C., McKey, D., & Douzery, E. J. P. (2004). Differentiation in a geographical mosaic of plants coevolving with ants: phylogeny of the Leonardoxa africana complex (Fabaceae: Caesalpinioideae) using amplified fragment length polymorphism markers. Molecular Ecology, 13(5), 1157–1171.

    Article  PubMed  CAS  Google Scholar 

  • Bruce, T. J. A., Wadhams, L. J., & Woodcock, C. M. (2005). Insect host location: A volatile situation. Trends in Plant Science, 10(6), 269–274.

    Article  PubMed  CAS  Google Scholar 

  • Bruneau, A., Forest, F., Herendeen, P. S., Klitgaard, B. B., & Lewis, G. P. (2001). Phylogenetic relationships in the Caesalpinioideae (Leguminosae) as inferred from chloroplast trnL intron sequences. Systematic Botany, 26(3), 487–514.

    Google Scholar 

  • Chenuil, A., & McKey, D. B. (1996). Molecular phylogenetic study of a myrmecophyte symbiosis: Did Leonardoxa/ant associations diversify via cospeciation? Molecular Phylogenetics and Evolution, 6(2), 270–286.

    Article  PubMed  CAS  Google Scholar 

  • Davidson, D. W., & McKey, D. (1993). The evolutionary ecology of symbiotic ant-plant relationships. Journal of Hymenoptera Research, 2, 13–83.

    Google Scholar 

  • D’Ettorre, P., Heinze, J., Schulz, C., Francke, W., & Ayasse, M. (2004). Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa. Journal of Experimental Biology, 207, 1085–1091.

    Article  PubMed  Google Scholar 

  • Dicke, M. (2009). Behavioural and community ecology of plants that cry for help. Plant Cell and Environment, 32(6), 654–665.

    Article  CAS  Google Scholar 

  • Gaume, L., McKey, D. (1998). Protection against herbivores of the myrmecophyte Leonardoxa africana (Baill.) Aubrèv. T3 by its principal ant inhabitant Aphomomyrmex afer Emery. Comptes Rendus de l’Academie des Sciences Serie III Sciences de la vie 321:593–601.

  • Gaume, L., & McKey, D. (1999). An ant-plant mutualism and its host-specific parasite: Activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant-ants inhabiting the same myrmecophyte. Oikos, 84, 130–144.

    Article  Google Scholar 

  • Gaume, L., McKey, D., & Anstett, M. C. (1997). Benefits conferred by “timid” ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax. Oecologia, 112, 209–216.

    Article  Google Scholar 

  • Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London Series B, 205(1161), 581–598.

    Article  CAS  Google Scholar 

  • Grangier, J., Dejean, A., Male, P. J., & Orivel, J. (2008). Indirect defense in a highly specific ant-plant mutualism. Naturwissenschaften, 95(10), 909–916.

    Article  PubMed  CAS  Google Scholar 

  • Heil, M. (2008). Indirect defence via tritrophic interactions. New Phytologist, 178(1), 41–61.

    Article  PubMed  CAS  Google Scholar 

  • Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6(2), 65–70.

    Google Scholar 

  • Huey, R. B., Gilchrist, G. W., Carlson, M. L., Berrigan, D., & Serra, L. (2000). Rapid evolution of a geographic cline in size in an introduced fly. Science, 287(5451), 308–309.

    Article  PubMed  CAS  Google Scholar 

  • Janzen, D. H. (1975). Pseudomyrmex nigropilosa: A parasite of mutualism. Science, 188(4191), 936–937.

    Article  PubMed  CAS  Google Scholar 

  • Léotard, G. (2007). Contribution à l’étude des facteurs responsables des grands patrons de biodiversité. Apports de l’étude du complexe de Leonardoxa africana (Fabaceae Université Montpellier II Caesalpinioideae), plante à fourmis des forêts pluviales du Cameroun. Montpellier, France: Université Montpellier II.

    Google Scholar 

  • Léotard, G., Saltmarsh, A., Kjellberg, F., & McKey, D. (2008). Mutualism, hybrid inviability and speciation in a tropical ant-plant. Journal of Evolutionary Biology, 21, 1133–1143.

    Article  PubMed  Google Scholar 

  • Letourneau, D. K. (1998). Ants, stem-borers, and fungal pathogens: Experimental tests of a fitness advantage in Piper ant-plants. Ecology, 79(2), 593–603.

    Google Scholar 

  • Lopez-Riquelme, G. O., Malo, E. A., Cruz-Lopez, L., & Fanjul-Moles, M. L. (2006). Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (Hymenoptera : Formicidae). Physiological Entomology, 31(4), 353–360.

    Article  CAS  Google Scholar 

  • Maynard-Smith, J. (1991). Honest signalling: The Philip Sidney game. Animal Behaviour, 42, 1034–1035.

    Article  Google Scholar 

  • McKey, D. (2000). Leonardoxa africana (Leguminosae: Caesalpinioideae): A complex of mostly allopatric subspecies. Adansonia, 22, 71–109.

    Google Scholar 

  • Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., & Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318(5847), 113–116.

    Article  PubMed  CAS  Google Scholar 

  • Raguso, R. A., & Light, D. M. (1998). Electroantennogram responses of male Sphinx perelegans hawkmoths to floral and ‘green-leaf volatiles’. Entomologia Experimentalis et Applicata, 86(3), 287–293.

    Article  CAS  Google Scholar 

  • Rico-Gray, V., & Oliveira, P. S. (2007). The ecology and evolution of ant-plant interactions (p. 331). Chicago: The University of Chicago Press.

    Google Scholar 

  • Rosumek, F. B., Silveira, F. A. O., Neves, F. D., Barbosa, N. P. D., Diniz, L., Oki, Y., et al. (2009). Ants on plants: A meta-analysis of the role of ants as plant biotic defenses. Oecologia, 160(3), 537–549.

    Article  PubMed  Google Scholar 

  • Schatz, B., Djieto-Lordon, C., Dormont, L., Bessiere, J. M., McKey, D., & Blatrix, R. (2009). A simple nonspecific chemical signal mediates defence behaviour in a specialised ant-plant mutualism. Current Biology, 19(9), R361–R362.

    Article  PubMed  CAS  Google Scholar 

  • Sheridan, S. L., Iversen, K. A., & Itagaki, H. (1996). The role of chemical senses in seed-carrying behavior by ants: A behavioral, physiological, and morphological study. Journal of Insect Physiology, 42(2), 149–159.

    Article  CAS  Google Scholar 

  • Shulaev, V., Silverman, P., & Raskin, I. (1997). Airborne signalling by methyl salicylate in plant pathogen resistance. Nature, 385(6618), 718–721.

    Article  CAS  Google Scholar 

  • Suarez, A. V., De Moraes, C. M., & Ippolito, A. (1998). Defense of Acacia collinsii by an obligate and nonobligate ant species: The significance of encroaching vegetation. Biotropica, 30(3), 480–482.

    Article  Google Scholar 

  • Takabayashi, J., Sabelis, M. W., Janssen, A., Shiojiri, K., & van Wijk, M. (2006). Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecological Research, 21(1), 3–8.

    Article  Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., & Lewis, W. J. (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250(4985), 1251–1253.

    Article  PubMed  CAS  Google Scholar 

  • Turlings, T. C. J., & Wäckers, F. (2004). Recruitment of predators and parasitoids by herbivore-injured plants. In R. T. Cardé & J. G. Millar (Eds.), Advances in insect chemical ecology (pp. 21–75). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Vaitkeviciene, G., Peteraitis, R., & Skirkeviciene, Z. (1994). Evaluation of air flow - pheromone carrier- effect on antennal receptors of bee Apis mellifera L. Pheromones, 4, 39–50.

    Google Scholar 

  • Vermeij, G. J. (1994). The evolutionary interaction among species: Selection, escalation, and coevolution. Annual Review of Ecology and Systematics, 25, 219–236.

    Article  Google Scholar 

  • Yu, D. W., & Pierce, N. E. (1998). A castration parasite of an ant-plant mutualism. Proceedings of the Royal Society of London Series B, 265, 375–382.

    Article  Google Scholar 

Download references

Acknowledgments

We are indebted to Michael Hochberg for commenting on an earlier version of the manuscript and to Finn Kjellberg for discussion about interpretation of the data. We also thank Michael Staudt, Renée Borges, Thomas Lenormand and Doug Yu for their comments on the manuscript. We thank the Ministry of Scientific Research and Innovation of the Republic of Cameroon for permission to carry out this study. Xavier Garde and the IRD in Yaoundé provided logistic help in the field. We thank Big John and his family and the traditional chief for their hospitality at the village of NkoloBondé, and Alain Ngomi for his help in the field in the village of Ebodjé. Laboratory experiments were conducted at the « Plate-forme d’Analyses Chimiques en Ecologie, plate-forme de l’IFR/SFR 119 Montpellier Environnement Biodiversité ». This study was funded by two grants from the French Agence Nationale de la Recherche: one from the “Young scientists” programme to R.B. (research agreement no. ANR-06-JCJC-0127) and one from the “Biodiversity” programme to D.M. and R.B. (IFORA project).

Author information

Authors and Affiliations

  1. Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), UMR 5175 (CNRS, Université Montpellier 2), 1919 route de Mende, 34293, Montpellier cedex 5, France

    Marion Vittecoq, Bruno Buatois, Laurent Dormont, Doyle McKey & Rumsaïs Blatrix

  2. Centre de Recherche de la Tour du Valat, Le Sambuc, 13200, Arles, France

    Marion Vittecoq

  3. Laboratory of Zoology, University of Yaoundé I, Faculty of Science, PO Box 812, Yaoundé, Cameroon

    Champlain Djieto-Lordon

Authors
  1. Marion Vittecoq
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Champlain Djieto-Lordon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruno Buatois
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laurent Dormont
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Doyle McKey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rumsaïs Blatrix
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rumsaïs Blatrix.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11692_2011_9125_MOESM1_ESM.doc

Figure S1: Antennal responses of ants (measured by electroantennography) to p-cymene (Cym), (E)-2-hexenol (E), hexanal (Hex), a mixture of E+Hex+MS (Mix), methyl salicylate (MS), and r-α-phellandrene (Phel). Intensity of antennal response is measured by the amplitude of depolarization (Dc) and expressed as the percentage of the corresponding putative control (Dtn) (Y axis: 100*Dc/Dtn, see text for details). The dashed line represents the level of the control (100%). Stars indicate compounds for which the antennal response is significantly (p<0.05) higher than response to the putative control (Wilcoxon tests comparing Dc and Dtn). (DOC 313 kb)

11692_2011_9125_MOESM2_ESM.doc

Figure S2: Antennal responses of ants (measured by electroantennography) to increasing amounts (0.4, 0.8, 4, 8, 36 and 400 nl, X axis) of methyl salicylate, hexanal, and (E)-2-hexenol. Intensity of antennal response is measured by the amplitude of depolarization (Dc) and expressed as the percentage of the corresponding putative control (Dtn) (Y axis: 100*Dc/Dtn, see text for details). The dashed line represents the level of the control (100%). Stars indicate quantities of compounds for which the antennal response was significantly (p<0.05) higher than response to the putative control (Wilcoxon tests comparing Dc and Dtn). (DOC 261 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vittecoq, M., Djieto-Lordon, C., Buatois, B. et al. The Evolution of Communication in Two Ant-Plant Mutualisms. Evol Biol 38, 360–369 (2011). https://doi.org/10.1007/s11692-011-9125-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-011-9125-8

Keywords

Search

Navigation