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EPHEMERAL WINDOWS OF OPPORTUNITY FOR HORIZONTAL TRANSMISSION OF FUNGAL SYMBIONTS IN LEAF-CUTTING ANTS

Authors

  • Michael Poulsen,

    1. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark
    2. Smithsonian Tropical Research Institute, Apartado 2072, Ancón, República de Panamá, STRI, Unit 9100, APO AA 34002-9998
    3. Department of Bacteriology, University of Wisconsin, Madison, 4325 Microbial Sciences Building, 1550 Linden Dr., Madison, Wisconsin 53706
    4. E-mail: Poulsen@bact.wisc.edu
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  • Hermógenes Fernández-Marín,

    1. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark
    2. Smithsonian Tropical Research Institute, Apartado 2072, Ancón, República de Panamá, STRI, Unit 9100, APO AA 34002-9998
    3. E-mail: FernandezH@si.edu
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  • Cameron R. Currie,

    1. Department of Bacteriology, University of Wisconsin, Madison, 4325 Microbial Sciences Building, 1550 Linden Dr., Madison, Wisconsin 53706
    2. E-mail: Currie@bact.wisc.edu
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  • Jacobus J. Boomsma

    1. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark
    2. E-mail: JJBoomsma@bio.ku.dk
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Abstract

Evolutionary theory predicts that hosts are selected to prevent mixing of genetically different symbionts when competition among lineages reduces the productivity of a mutualism. The symbionts themselves may also defend their interests: recent studies of Acromyrmex leaf-cutting ants showed that somatic incompatibility enforces single-clone gardens within mature colonies, thereby constraining horizontal transmission of fungal symbionts. However, phylogenetic analyses indicate that symbiont switches occur frequently enough to remove most signs of host-symbiont cocladogenesis. Here we resolve this paradox by showing that transmission among newly founded Acromyrmex colonies is not constrained. All tested queens of sympatric A. octospinosus and A. echinatior offered a novel fragment of fungus garden accepted the new symbiont. The outcome was unaffected by genetic distance between the novel and the original symbiont, and by the ant species the novel symbiont came from. The colony founding stage may thus provide an efficient but transient window for horizontal transmission, in which the fungus is unable to actively defend its partnership position before the host feeds on it, so that host fecal droplets remain compatible with alternative strains during the early stage of colony founding. We discuss how brief stages of low commitment between partners may increase the evolutionary stability of ancient coevolved mutualisms.

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