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What makes you a potential partner? Insights from convergently evolved ant–ant symbioses

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Abstract

Mutualistic, commensalistic or parasitic interactions are unevenly distributed across the animals and plants: in certain taxa, such interspecific associations evolved more often than in others. Within the ants, associations between species of the genera Camponotus and Crematogaster evolved repeatedly and include trail-sharing associations, where two species share foraging trails, and parabioses, where two species share a nest without aggression. Camponotus and Crematogaster may possess life-history traits that favour the evolution of associations. To identify which traits are affected by the association, we investigated a neotropical parabiosis of Ca. femoratus and Cr. levior and compared it to a paleotropical parabiosis and a trail-sharing association. The two neotropical species showed altered cuticular hydrocarbon profiles compared to non-parabiotic species accompanied by low levels of interspecific aggression. Both species occurred in two chemically distinct types. Camponotus followed artificial trails of Crematogaster pheromones, but not vice versa. The above traits were also found in the paleotropical parabiosis, and the trail-following results match those of the trail-sharing association. In contrast to paleotropical parabioses, however, Camponotus was dominant, had a high foraging activity and often fought against Crematogaster over food resources. We suggest three potential preadaptations for parabiosis. First, Crematogaster uses molecules as trail pheromones, which can be perceived by Camponotus, too. Second, nests of Camponotus are an important benefit to Crematogaster and may create a selection pressure for the latter to tolerate Camponotus. Third, there are parallel, but unusual, shifts in cuticular hydrocarbon profiles between neotropics and paleotropics, and between Camponotus and Crematogaster.

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Acknowledgments

We are grateful to the Laboratoire Environnement de Petit Saut for furnishing logistical support and the Les Nouragues Research Station for research permission. This work has benefited from an “Investissement d’Avenir” grant managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-0025).

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Authors and Affiliations

  1. Department of Evolutionary Biology, Institute of Zoology, University of Mainz, Johannes-von-Müller-Weg 6, 55099, Mainz, Germany

    Florian Menzel

  2. UMR 8172 Ecologie de Forêts de Guyane (EcoFoG), CNRS, Campus Agronomique, BP 316, 97379, Kourou Cedex, France

    Jérôme Orivel

  3. Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany

    Martin Kaltenpoth

  4. Department of Animal Ecology and Tropical Biology Biocentre, University of Würzburg, Am Hubland, 97074, Würzburg, Germany

    Thomas Schmitt

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  1. Florian Menzel
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Correspondence to Florian Menzel.

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Handling Editor: Michael Heethoff.

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Supplemental figures: Fig. S1 Substance class by chain length for each of the samples analysed. Each barplot represents one colony. The bars give the relative abundance of CHC, separated by chain length and with different colours for each substance class. The bars of each barplot add up to 100 %. Note that the graphs do not show differences between methyl group positions or (for alkenes) retention times among substances of the same chain length.

Fig. S2 NMDS ordination of CHC of Crematogaster levior, Cr. carinata and Camponotus femoratus.

Supplemental Tables Table S1. Cuticular hydrocarbons of Camponotus femoratus, Crematogaster levior and Crematogaster carinata. Each column represents one colony, with collection site and colony code given above. The numbers give the relative abundance of each substance.

Table S2. PERMANOVA results from aggression assays for the four species combinations. The aggression index was determined for the aggression of residents towards an intruder; species combination is given as ‘resident-intruder’.

Table S3. Results for foraging ecology, data from Vantaux et al. (2007).

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Menzel, F., Orivel, J., Kaltenpoth, M. et al. What makes you a potential partner? Insights from convergently evolved ant–ant symbioses. Chemoecology 24, 105–119 (2014). https://doi.org/10.1007/s00049-014-0149-2

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