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Biology of the relict fungus-farming ant Apterostigma megacephala Lattke, including descriptions of the male, gyne, and larva

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Abstract

Fungus-farming “attine” ant agriculture consists of five distinct agricultural systems characterized by a remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Across-system garden switching experiments result in colony decline and death, indicating that attine ant-fungus symbiont fidelity is enforced by poorly understood biological constraints. The most dramatic violation of this pattern of symbiont fidelity occurs in the relict species Apterostigma megacephala, the only lower-attine ant known to cultivate a higher-attine fungus. Apterostigma megacephala is the sole surviving representative of an ancient lineage that diverged from all other Apterostigma fungus-farming ants ~39 million years ago, yet it cultivates Leucoagaricus gongylophorus, a highly domesticated fungal species that originated in the gardens of the recently evolved leaf-cutting ants 8–11 million years ago. Understanding the biology of A. megacephala, therefore, may provide important clues about the biological mechanisms that constrain the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture. Here, based on field work in the Floresta Nacional de Carajás in the state of Pará in Brazil, we report the previously unknown biology of A. megacephala, including nest architecture, colony demography, foraging behavior, and the morphologies of the previously undescribed gyne, male, and larva.

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Acknowledgements

We are grateful to R. C. F. Brandão and R. Rosa da Silva for information about Apterostigma megacephala in Carajás; to T. Izzo for information about A. megacephala in Juara, Mato Grosso; to J. Chaúl (Universidade Federal de Viçosa) for information regarding collections of A. megacephala in Canarana, Mato Grosso; to F. Drumond Martins and E. Esteves of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) at Floresta Nacional de Carajás for their help and guidance; to E. Okonski (NMNH) for collections and research support; to S. Messer (University of Rochester) for help with the description of the male genitalia, and to S. Whittaker (NMNH) for help with preparation of the larvae. This manuscript was greatly improved thanks to comments from Terry McGlynn and two anonymous reviewers. For permission to conduct field research, we thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Processo EXC 039/07; Portarias 267, 359), the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), and the ICMBio (permits 14789-1, 14789-2). J. S.-C., C. R., and T. R. S. were supported by National Science Foundation (NSF) Grants (DEB-1456964 and DEB-1654829), T. R. S. and J. S.-C. were supported by National Science Foundation (NSF) Grant DEB-0949689, and the National Museum of Natural History (NMNH) Small Grants program; T. R. S. by the Smithsonian Institution Scholarly Studies Program; J. S.-C. and A. J. by NMNH Peter Buck Predoctoral Fellowships and Max and Vera Britton Environmental Science Awards (Cosmos Club Foundation); and M. B. and A. R. by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; 2011/50226-0; 2014/24298-1, respectively) and CNPq (311562/2012-4 and 487639/2012-0).

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  1. J. Sosa-Calvo & C. Rabeling

    Present address: Center for Social Insect Research, School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA

Authors and Affiliations

  1. Department of Biology, University of Rochester, Rochester, NY, 14627, USA

    J. Sosa-Calvo & C. Rabeling

  2. Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013, USA

    J. Sosa-Calvo, A. Ješovnik & T. R. Schultz

  3. Maryland Center for Systematic Entomology, Department of Entomology, University of Maryland, College Park, MD, 20782, USA

    A. Ješovnik

  4. Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil

    C. T. Lopes & H. L. Vasconcelos

  5. Centro de Estudos de Insetos Sociais, Universidade Estadual Paulista UNESP, Rio Claro, São Paulo, Brazil

    A. Rodrigues & M. Bacci Jr.

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  1. J. Sosa-Calvo
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Sosa-Calvo, J., Ješovnik, A., Lopes, C.T. et al. Biology of the relict fungus-farming ant Apterostigma megacephala Lattke, including descriptions of the male, gyne, and larva. Insect. Soc. 64, 329–346 (2017). https://doi.org/10.1007/s00040-017-0550-2

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