Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

University of Wisconsin–Madison, Madison, Wisconsin, United States
The ISME Journal (Impact Factor: 9.3). 09/2007; 1(4):313-20. DOI: 10.1038/ismej.2007.41
Source: PubMed


Symbiont choice has been proposed to play an important role in shaping many symbiotic relationships, including the fungus-growing ant-microbe mutualism. Over millions of years, fungus-growing ants have defended their fungus gardens from specialized parasites with antibiotics produced by an actinomycete bacterial mutualist (genus Pseudonocardia). Despite the potential of being infected by phylogenetically diverse strains of parasites, each ant colony maintains only a single Pseudonocardia symbiont strain, which is primarily vertically transmitted between colonies by the founding queens. In this study, we show that Acromyrmex leaf-cutter ants are able to differentiate between their native actinomycete strain and a variety of foreign strains isolated from sympatric and allopatric Acromyrmex species, in addition to strains originating from other fungus-growing ant genera. The recognition mechanism is sufficiently sensitive for the ants to discriminate between closely related symbiont strains. Our findings suggest that symbiont recognition may play a crucial role in the fungus-growing ant-bacterium mutualism, likely allowing the ants to retain ecological flexibility necessary for defending their garden from diverse parasites and, at the same time, resolve potential conflict that can arise from rearing competing symbiont strains.

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Available from: Michael Poulsen
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    • "Mechanisms of partner choice include both favoring more beneficial symbionts (e.g., Zhang et al. 2007) and punishing less beneficial or more costly partners (often called sanctions; e.g., Kiers et al. 2003). In each case, partner choice establishes a positive covariance "
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    ABSTRACT: While past work has often examined the effects of transmission mode on virulence evolution in parasites, few studies have explored the impact of horizontal transmission on the evolution of benefits conferred by a symbiont to its host. Here, we identify three mechanisms that create a positive covariance between horizontal transmission and symbiont-provided benefits: pleiotropy within the symbiont genome, partner choice by the host, and consumption of host waste by-products by symbionts. We modify a susceptible-infected model to incorporate the details of each mechanism and examine the evolution of symbiont benefits given variation in either the immigration rate of susceptible hosts or the rate of successful vertical transmission. We find conditions for each case under which greater opportunity for horizontal transmission (higher migration rate) favors the evolution of mutualism. Further, we find the surprising result that vertical transmission can inhibit the evolution of benefits provided by symbionts to hosts when horizontal transmission and symbiont-provided benefits are positively correlated. These predictions may apply to a number of natural systems, and the results may explain why many mutualisms that rely on partner choice often lack a mechanism for vertical transmission.
    Full-text · Article · Sep 2014 · Ecology and Evolution
    • "2011 ) , suggesting that partner choice plays an important role in maintaining the association over evolutionary timescales . Concordantly , bioassays with four Acromyrmex species indicated that the ants can differenti - ate their native microbial symbiont from other Pseudono - cardia strains ( Zhang , Poulsen & Currie 2007 ) . Additionally , there is some evidence that the ants prefer closely related over phylogenetically more distant Pseud - onocardia strains , regardless of whether the bacteria were previously ant associated or free living ( Poulsen et al . "
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    ABSTRACT: In all stages of their life cycle, insects are threatened by a multitude of predators, parasites, parasitoids and pathogens. The lifestyles and feeding ecologies of some hymenopteran taxa render them especially vulnerable to pathogen infestation. Specifically, development in sub-terranean brood cells, mass provisioning of resources for the offspring and the life of social insects in large communities can enhance the risk of pathogen infestation and/or the spread of disease among conspecifics.To counteract these threats, insects have evolved mechanical, chemical and behavioural defences as well as a complex immune system. In addition to the host's own defences, some Hymenoptera are associated with protective symbionts. Leaf-cutting ants, solitary digger wasps, bees and bumblebees engage in symbiotic interactions with bacteria that protect the adult host, the developing offspring or the food resources against microbial infections. In the well-studied cases of ants and wasps, the protective activity is mediated by the production of antimicrobial secondary metabolites. In other symbiotic interactions, however, competitive exclusion and immune priming may also play an important role in enhancing protection. Phylogenetic studies indicate that the defensive associations in Hymenoptera are generally more dynamic than the intimate nutritional mutualisms, with horizontal transfer or de novo uptake of the symbionts from the environment occurring frequently.Mutualistic micro-organisms can also significantly influence the outcome of host-parasitoid interactions. Some insects are protected by symbiont-produced toxins against parasitic wasps. Ichneumonid and braconid parasitoids, on the other hand, are associated with symbiotic viruses that are injected into the caterpillar host during oviposition and suppress its immune system to the advantage of the parasitoid.The increasing affordability of next-generation sequencing technologies will greatly facilitate the analysis of insect-associated microbial communities and undoubtedly uncover a plethora of as yet unknown protective symbioses. However, a detailed understanding of the host's natural history is indispensable for elucidating the fitness benefits of the symbionts and the molecular basis of symbiont-conferred protection.
    No preview · Article · Apr 2014 · Functional Ecology
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    • "), as well as discriminate between native and non-native 54 protective bacterial Pseudonocardia symbionts (Zhang et al. 2007), thus allowing "

    Full-text · Article · Feb 2014 · Journal of Chemical Ecology
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