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Evolutionary transition from single to multiple mating in fungus-growing ants

Authors

  • P. Villesen,

    Corresponding author
    1. Department of Ecology & Genetics, University of Aarhus, DK-8000 Aarhus C, Denmark,
      P. Villesen, Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, 8000 Aarhus C, Denmark. Fax: +45 86127191; E-mail:Palle.Villesen@biology.au.dk
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  • P. J. Gertsch,

    1. Department of Conservation Biology and Genetics, Evolutionary Biology Centre, Uppsala University, Box 7003, S-750 07 Uppsala, Sweden,
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  • J. Frydenberg,

    1. Department of Ecology & Genetics, University of Aarhus, DK-8000 Aarhus C, Denmark,
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  • U. G. Mueller,

    1. Section of Integrative Biology, Patterson Laboratories, University of Texas, Austin, TX 78713, USA,
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  • J. J. Boomsma

    1. Department of Ecology & Genetics, University of Aarhus, DK-8000 Aarhus C, Denmark,
    2. Zoological Institute, Department of Population Ecology, University of Copenhagen, DK-2100 Copenhagen East, Denmark
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P. Villesen, Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, 8000 Aarhus C, Denmark. Fax: +45 86127191; E-mail:Palle.Villesen@biology.au.dk

Abstract

Queens of leafcutter ants exhibit the highest known levels of multiple mating (up to 10 mates per queen) among ants. Multiple mating may have been selected to increase genetic diversity among nestmate workers, which is hypothesized to be critical in social systems with large, long-lived colonies under severe pressure of pathogens. Advanced fungus-growing (leafcutter) ants have large numbers (104–106 workers) and long-lived colonies, whereas basal genera in the attine tribe have small (< 200 workers) colonies with probably substantially shorter lifespans. Basal attines are therefore expected to have lower queen mating frequencies, similar to those found in most other ants. We tested this prediction by analysing queen mating frequency and colony kin structure in three basal attine species: Myrmicocrypta ednaella, Apterostigma collare and Cyphomyrmex longiscapus. Microsatellite marker analyses revealed that queens in all three species were single mated, and that worker-to-worker relatedness in these basal attine species is very close to 0.75, the value expected under exclusively single mating. Fungus growing per se has therefore not selected for multiple queen mating. Instead, the advanced and highly productive social structure of the higher attine ants, which is fully dependent on the rearing of an ancient clonal fungus, may have necessitated high genetic diversity among nestmate workers. This is not the case in the lower attines, which rear fungi that were more recently derived from free-living fungal populations.

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