Article

Symbiotic adaptations in the fungal cultivar of leaf-cutting ants

  • Nature Communications 5, Article number: 5675 (2014)
  • doi:10.1038/ncomms6675
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Abstract

Centuries of artificial selection have dramatically improved the yield of human agriculture; however, strong directional selection also occurs in natural symbiotic interactions. Fungus-growing attine ants cultivate basidiomycete fungi for food. One cultivar lineage has evolved inflated hyphal tips (gongylidia) that grow in bundles called staphylae, to specifically feed the ants. Here we show extensive regulation and molecular signals of adaptive evolution in gene trancripts associated with gongylidia biosynthesis, morphogenesis and enzymatic plant cell wall degradation in the leaf-cutting ant cultivar Leucoagaricus gongylophorus. Comparative analysis of staphylae growth morphology and transcriptome-wide expressional and nucleotide divergence indicate that gongylidia provide leaf-cutting ants with essential amino acids and plant-degrading enzymes, and that they may have done so for 20–25 million years without much evolutionary change. These molecular traits and signatures of selection imply that staphylae are highly advanced coevolutionary organs that play pivotal roles in the mutualism between leaf-cutting ants and their fungal cultivars.

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Acknowledgements

We thank the Smithsonian Tropical Research Institute (STRI) for providing logistic help and facilities to work in Gamboa, the Autoridad Nacional del Ambiente y el Mar (ANAM) for permission to sample ants in Panama and to export them to Denmark, the Swedish National Infrastructure for Computing (SNIC) at the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) for access and use of computing resources (project: b2012090), Björn Canbäck and Dag Ahrén for helpful discussion of bioinformatics analyses, Eva Friman and Tomas Johansson for laboratory support with sequencing, and Rachelle Adams and Joanito Liberti for help and collaboration with field work. This study was supported by a postdoctoral fellowship from The Danish Council for Independent Research|Natural Sciences to HHDFL, by a grant of the Danish National Research Foundation (DNRF57) to J.J.B., and by a grant from the Swedish Research Council (VR) to A.T.

Author information

Author notes

    • Henrik H. De Fine Licht

    Present Address: Section for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg, Denmark

Affiliations

  1. Microbial Ecology Group, Department of Biology, Lund University, Ecology Building, SE-223 62 Lund, Sweden

    • Henrik H. De Fine Licht
    •  & Anders Tunlid
  2. Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark

    • Jacobus J. Boomsma

Authors

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Contributions

Conceived and designed the experiments: H.H.D.F.L. and A.T. Performed the experimental work and analysed the data: H.H.D.F.L. Contributed new reagents and biological material: J.J.B. Wrote the paper: H.H.D.F.L., J.J.B. and A.T.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Henrik H. De Fine Licht.

Supplementary information

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    Supplementary Information

    Supplementary Figures 1-4, Supplementary Tables 1-10, Supplementary Discussion and Supplementary References.

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