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Instability of novel ant-fungal associations constrains horizontal exchange of fungal symbionts

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Abstract

One of the more fascinating features of fungus-gardening ants (Attini: Formicidae) is their fidelity to their lineage-specific fungal symbionts. Among the derived higher-attine ants (leafcutter ants and close relatives), it is thought that most leaf-cutting ants grow Attamyces fungus whereas most Trachymyrmex ants grow ‘Trachymyces’ fungus, but there exist exceptions to this clade-to-clade correspondence between ants and fungi. The exceptions are inconsistent with strict one-to-one coevolution, which suggests that ants sometimes are able to switch to novel fungi. Such switches appear to be largely constrained and ants are generally faithful to their species-specific fungi. Prior experiments demonstrated no clear fitness consequences of growing novel fungi over the short-term when the ant Trachymyrmex septentrionalis was symbiont-switched by forcing it to grow Attamyces leaf-cutter fungus. We hypothesized that long-term ant-fungal fidelity is constrained either by physiological differences among fungal species or by garden diseases that symbiont-switched ants cannot control. Repeat experiments in a different location show that T. septentrionalis colonies switched to grow Attamyces exhibit sudden declines in garden biomass and consequent fitness reductions due to garden destruction by pathogens, whereas control colonies (Trachymyrmex ants cultivating Trachymyces fungus) do not show parallel garden declines. These patterns are mirrored in symbiont-switch experiments conducted on colonies in Trachymyrmex turrifex. Disease microbes selecting on ant-cultivar combinations therefore can constrain switches to novel cultivars and maintain combinations that are more resistant to disease.

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Acknowledgments

Constructive comments by the reviewers and editors greatly improved the manuscript. We also thank Andre Rodrigues for sharing his knowledge about attine-garden weeds; Walter Tschinkel for use of his laboratory; and John Crutchfield, Larry Gilbert, and Steven Gibson for facilitating the colony collections at Brackenridge Field Laboratory and at Stengl Lost Pines Field Station. The USDA Forest Service allowed us to collect colonies in the Apalachicola National Forest. Funding was provided by NSF award IOS-0920138 to JNS and UGM.

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  1. Integrative Biology, University of Texas at Austin, 1 University Station #C0930, Austin, TX, 78712, USA

    U. G. Mueller

  2. Department of Biology, University of Texas at Tyler, 3900 University Blvd, Tyler, TX, 75701, USA

    Jon N. Seal

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Seal, J.N., Mueller, U.G. Instability of novel ant-fungal associations constrains horizontal exchange of fungal symbionts. Evol Ecol 28, 157–176 (2014). https://doi.org/10.1007/s10682-013-9665-8

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