Abstract
Conflict within mutually beneficial associations is predicted to destabilize relationships, and theoretical and empirical work exploring this has provided significant insight into the dynamics of cooperative interactions. Within mutualistic associations, the expression and regulation of conflict is likely more complex than in intraspecific cooperative relationship, because of the potential presence of: i) multiple genotypes of microbial species associated with individual hosts, ii) multiple species of symbiotic lineages forming cooperative partner pairings, and iii) additional symbiont lineages. Here we explore complexity of conflict expression within the ancient and coevolved mutualistic association between attine ants, their fungal cultivar, and actinomycetous bacteria (Pseudonocardia). Specifically, we examine conflict between the ants and their Pseudonocardia symbionts maintained to derive antibiotics against parasitic microfungi (Escovopsis) infecting the ants' fungus garden. Symbiont assays pairing isolates of Pseudonocardia spp. associated with fungus-growing ants spanning the phylogenetic diversity of the mutualism revealed that antagonism between strains is common. In contrast, antagonism was substantially less common between more closely related bacteria associated with Acromyrmex leaf-cutting ants. In both experiments, the observed variation in antagonism across pairings was primarily due to the inhibitory capabilities and susceptibility of individual strains, but also the phylogenetic relationships between the ant host of the symbionts, as well as the pair-wise genetic distances between strains. The presence of antagonism throughout the phylogenetic diversity of Pseudonocardia symbionts indicates that these reactions likely have shaped the symbiosis from its origin. Antagonism is expected to prevent novel strains from invading colonies, enforcing single-strain rearing within individual ant colonies. While this may align ant-actinomycete interests in the bipartite association, the presence of single strains of Pseudonocardia within colonies may not be in the best interest of the ants, because increasing the diversity of bacteria, and thereby antibiotic diversity, would help the ant-fungus mutualism deal with the specialized parasites.
Highlights
Mutually beneficial associations appear congenial, selection favoring individual partners using resources to facilitate their own selfish interests is predicted to destabilize cooperation [e.g. 1]; a paradox known as ‘‘the tragedy of the commons’’ [1,2]
The widespread ability of ant-associated Pseudonocardia to inhibit other symbiont strains suggest that competitive conflict will often be expressed when actinomycete strains mix and thereby may directly impact host-symbiont dynamics
Our results indicate that Pseudonocardia bacteria have the capacity to inhibit other Pseudonocardia strains, there was abundant variation in both the ability to inhibit other strains and in the resistance to compounds
Summary
Mutually beneficial associations appear congenial, selection favoring individual partners using resources to facilitate their own selfish interests is predicted to destabilize cooperation [e.g. 1]; a paradox known as ‘‘the tragedy of the commons’’ [1,2]. This inherent conflict is recognized as shaping both within- and between-species cooperative relationships [3,4,5,6], and extensive theoretical and empirical studies examining conflict within intraspecific cooperative relationships have provided important insights into social evolution and the stability of cooperation [e.g., 3, 7–8]. The presence of host sanctions directed towards cheating symbionts has been identified in several mutualisms [e.g., 17–20]
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