Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

Department of Bacteriology, University of Wisconsin-Madison, Madison, WI 53706, USA.
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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    • "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.
    Ecology and Evolution 09/2014; 4(17). DOI:10.1002/ece3.1166 · 2.32 Impact Factor
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    • "), as well as discriminate between native and non-native 54 protective bacterial Pseudonocardia symbionts (Zhang et al. 2007), thus allowing "
    Journal of Chemical Ecology 02/2014; 40(2). DOI:10.1007/s10886-014-0382-8 · 2.75 Impact Factor
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    • "In a recent report, Zhang et al. (2007) conducted behavioral experiments and showed that Acromyrmex workers are able to differentiate between their native and a foreign Pseudonocardia strain, and proposed that this could explain the potential exclusion of additional Pseudonocardia strains. However, the Zhang et al. (2007) study focused on preference between native versus non-native strains but did not elucidate ant preference when workers are challenged with two nonnative Pseudonocardia strains. "
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    ABSTRACT: Fungus-growing ants display symbiont preference in behavioral assays, both towards the fungus they cultivate for food and Actinobacteria they maintain on their cuticle for antibiotic production against parasites. These Actinobacteria, genus Pseudonocardia Henssen (Pseudonocardiacea: Actinomycetales), help defend the ants' fungal mutualist from specialized parasites. In Acromyrmex Mayr (Hymenoptera: Formicidae) leaf-cutting ants, individual colonies maintain either a single or a few strains of Pseudonocardia, and the symbiont is primarily vertically transmitted between generations by colony-founding queens. A recent report found that Acromyrmex workers are able to differentiate between their native Pseudonocardia strain and non-native strains isolated from sympatric or allopatric Acromyrmex species, and show preference for their native strain. Here we explore worker preference when presented with two non-native strains, elucidating the role of genetic distance on preference between strains and Pseudonocardia origin. Our findings suggest that ants tend to prefer bacteria more closely related to their native bacterium and that genetic similarity is probably more important than whether symbionts are ant-associated or free-living. Preliminary findings suggest that when continued exposure to a novel Pseudonocardia strain occurs, ant symbiont preference is potentially adaptable, with colonies apparently being able to alter symbiont preference over time. These findings are discussed in relation to the role of adaptive recognition, potential ecological flexibility in symbiont preference, and more broadly, in relation to self versus non-self recognition.
    Journal of Insect Science 09/2011; 11(120):120. DOI:10.1673/031.011.12001 · 1.03 Impact Factor
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