Abstract

The stability of mutualistic interactions is likely to be affected by the genetic diversity of symbionts that compete for the same functional niche. Fungus-growing (attine) ants have multiple complex symbioses and thus provide ample opportunities to address questions of symbiont specificity and diversity. Among the partners are Actinobacteria of the genus Pseudonocardia that are maintained on the ant cuticle to produce antibiotics, primarily against a fungal parasite of the mutualistic gardens. The symbiosis has been assumed to be a hallmark of evolutionary stability, but this notion has been challenged by culturing and sequencing data indicating an unpredictably high diversity. We used 454 pyrosequencing of 16S rRNA to estimate the diversity of the cuticular bacterial community of the leaf-cutting ant Acromyrmex echinatior and other fungus-growing ants from Gamboa, Panama. Both field and laboratory samples of the same colonies were collected, the latter after colonies had been kept under laboratory conditions for up to 10 years. We show that bacterial communities are highly colony-specific and stable over time. The majority of colonies (25/26) had a single dominant Pseudonocardia strain, and only two strains were found in the Gamboa population across 17 years, confirming an earlier study. The microbial community on newly hatched ants consisted almost exclusively of a single strain of Pseudonocardia while other Actinobacteria were identified on older, foraging ants in varying but usually much lower abundances. These findings are consistent with recent theory predicting that mixtures of antibiotic-producing bacteria can remain mutualistic when dominated by a single vertically transmitted and resource-demanding strain.

Highlights

  • Questions of conflict and cooperation are fundamental for understanding the evolutionary stability of genomes, societies and inter-specific mutualisms (Herre et al 1999; Burt & Trivers 2006; Bourke 2011; Scheuring & Yu 2012; Schluter & Foster 2012)

  • Our analyses of the diversity of bacterial communities identified two Pseudonocardia strains that dominated the cuticular diversity of Acromyrmex echinatior, and these almost never co-occurred in the same colony or on the same ants

  • Varying densities of Pseudonocardia bacteria were found in these samples, but without estimates of the total bacterial density, it was not possible to infer whether the densities of these vertically acquired Pseudonocardia were negatively correlated with densities of other Actinomycetales, as would be expected when strains compete (Scheuring & Yu 2012)

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Summary

Introduction

Questions of conflict and cooperation are fundamental for understanding the evolutionary stability of genomes, societies and inter-specific mutualisms (Herre et al 1999; Burt & Trivers 2006; Bourke 2011; Scheuring & Yu 2012; Schluter & Foster 2012). This is apparent when considering multispecies symbioses consisting of a mixture of mutualistic and parasitic partners with potentially diverging fitness interests, such as microbial gut communities (Qin et al 2010), nitrogenfixing bacteria of legumes (Kiers et al 2003) and microparasites of wild voles (Telfer et al 2010).

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