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Reciprocal genomic evolution in the ant–fungus agricultural symbiosis

Author

Listed:
  • Sanne Nygaard

    (Centre for Social Evolution, University of Copenhagen)

  • Haofu Hu

    (China National Genbank, BGI-Shenzhen)

  • Cai Li

    (China National Genbank, BGI-Shenzhen)

  • Morten Schiøtt

    (Centre for Social Evolution, University of Copenhagen)

  • Zhensheng Chen

    (China National Genbank, BGI-Shenzhen)

  • Zhikai Yang

    (China National Genbank, BGI-Shenzhen)

  • Qiaolin Xie

    (China National Genbank, BGI-Shenzhen)

  • Chunyu Ma

    (China National Genbank, BGI-Shenzhen)

  • Yuan Deng

    (China National Genbank, BGI-Shenzhen)

  • Rebecca B. Dikow

    (Smithsonian Institute for Biodiversity Genomics, Smithsonian Institution)

  • Christian Rabeling

    (University of Rochester
    National Museum of Natural History, Smithsonian Institution)

  • David R. Nash

    (Centre for Social Evolution, University of Copenhagen)

  • William T. Wcislo

    (Smithsonian Tropical Research Institute)

  • Seán G. Brady

    (National Museum of Natural History, Smithsonian Institution)

  • Ted R. Schultz

    (National Museum of Natural History, Smithsonian Institution)

  • Guojie Zhang

    (Centre for Social Evolution, University of Copenhagen
    China National Genbank, BGI-Shenzhen
    State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences)

  • Jacobus J. Boomsma

    (Centre for Social Evolution, University of Copenhagen)

Abstract

The attine ant–fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55–60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture.

Suggested Citation

  • Sanne Nygaard & Haofu Hu & Cai Li & Morten Schiøtt & Zhensheng Chen & Zhikai Yang & Qiaolin Xie & Chunyu Ma & Yuan Deng & Rebecca B. Dikow & Christian Rabeling & David R. Nash & William T. Wcislo & Se, 2016. "Reciprocal genomic evolution in the ant–fungus agricultural symbiosis," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12233
    DOI: 10.1038/ncomms12233
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    Cited by:

    1. Giacomo Moggioli & Balig Panossian & Yanan Sun & Daniel Thiel & Francisco M. Martín-Zamora & Martin Tran & Alexander M. Clifford & Shana K. Goffredi & Nadezhda Rimskaya-Korsakova & Gáspár Jékely & Mar, 2023. "Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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