Chemically armed mercenary ants protect fungus-farming societies

Edited by Bert Hölldobler, Arizona State University, Tempe, AZ, and approved August 4, 2013 (received for review June 20, 2013)
September 9, 2013
110 (39) 15752-15757

Significance

We document the behavioral interactions among three ant species: a fungus-growing host ant, a permanently associated parasitic guest ant, and a raiding agro-predator ant. We show that the presence of guest ants becomes advantageous when host ants are attacked by raider ants, because guest ants use alkaloid venom to defend their host ant colony. Furthermore, detection of the guest ant odors is sufficient to discourage raider scouts from recruiting nestmates to host colonies. Guest ants likely have evolved this protective behavior because they also perish when their host colony dies.

Abstract

The ants are extraordinary in having evolved many lineages that exploit closely related ant societies as social parasites, but social parasitism by distantly related ants is rare. Here we document the interaction dynamics among a Sericomyrmex fungus-growing ant host, a permanently associated parasitic guest ant of the genus Megalomyrmex, and a raiding agro-predator of the genus Gnamptogenys. We show experimentally that the guest ants protect their host colonies against agro-predator raids using alkaloid venom that is much more potent than the biting defenses of the host ants. Relatively few guest ants are sufficient to kill raiders that invariably exterminate host nests without a cohabiting guest ant colony. We also show that the odor of guest ants discourages raider scouts from recruiting nestmates to host colonies. Our results imply that Sericomyrmex fungus-growers obtain a net benefit from their costly guest ants behaving as a functional soldier caste to meet lethal threats from agro-predator raiders. The fundamentally different life histories of the agro-predators and guest ants appear to facilitate their coexistence in a negative frequency-dependent manner. Because a guest ant colony is committed for life to a single host colony, the guests would harm their own interests by not defending the host that they continue to exploit. This conditional mutualism is analogous to chronic sickle cell anemia enhancing the resistance to malaria and to episodes in human history when mercenary city defenders offered either net benefits or imposed net costs, depending on the level of threat from invading armies.

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Acknowledgments

We thank the staff and researchers at the Smithsonian Tropical Research Institute for help with logistics and facilities, the Autoridad Nacional del Ambiente y el Mar for permission to sample ants in Panama and export them to Denmark, Friluftsland A/S and John B. Anderson for equipment, and Rozlyn E. Haley for the ant drawings. We also thank two anonymous reviewers for comments and suggestions that improved this article. This work was funded by a Marie Curie International Incoming Fellowship [237266–evolutionAry traNsitions: Chemical Ecology of Parasitic Societies (ANCEPS), to R.M.M.A.], a Smithsonian Molecular Evolution Postdoctoral Fellowship (to R.M.M.A.), and a grant from the Danish National Research Foundation (DNRF57, to J.J.B.).

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 110 | No. 39
September 24, 2013
PubMed: 24019482

Classifications

Submission history

Published online: September 9, 2013
Published in issue: September 24, 2013

Keywords

  1. evolutionary transition
  2. symbiosis
  3. Attini
  4. Solenopsidini

Acknowledgments

We thank the staff and researchers at the Smithsonian Tropical Research Institute for help with logistics and facilities, the Autoridad Nacional del Ambiente y el Mar for permission to sample ants in Panama and export them to Denmark, Friluftsland A/S and John B. Anderson for equipment, and Rozlyn E. Haley for the ant drawings. We also thank two anonymous reviewers for comments and suggestions that improved this article. This work was funded by a Marie Curie International Incoming Fellowship [237266–evolutionAry traNsitions: Chemical Ecology of Parasitic Societies (ANCEPS), to R.M.M.A.], a Smithsonian Molecular Evolution Postdoctoral Fellowship (to R.M.M.A.), and a grant from the Danish National Research Foundation (DNRF57, to J.J.B.).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Rachelle M. M. Adams1 [email protected]
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560; and
Joanito Liberti
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
Anders A. Illum
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
Tappey H. Jones
Department of Chemistry, Virginia Military Institute, Lexington, VA 24450
David R. Nash1 [email protected]
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
Jacobus J. Boomsma
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;

Notes

1
To whom correspondence may be addressed. E-mail: [email protected] or [email protected].
Author contributions: R.M.M.A., J.L., A.A.I., D.R.N., and J.J.B. designed research; R.M.M.A., J.L., A.A.I., and T.H.J. performed research; R.M.M.A. and D.R.N. analyzed data; and R.M.M.A., D.R.N., and J.J.B. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Chemically armed mercenary ants protect fungus-farming societies
    Proceedings of the National Academy of Sciences
    • Vol. 110
    • No. 39
    • pp. 15503-15849

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