A Brazilian population of the asexual fungus-growing ant Mycocepurus smithii (Formicidae, Myrmicinae, Attini) cultivates fungal symbionts with gongylidia-like structures

PLoS One. 2014 Aug 7;9(8):e103800. doi: 10.1371/journal.pone.0103800. eCollection 2014.

Abstract

Attine ants cultivate fungi as their most important food source and in turn the fungus is nourished, protected against harmful microorganisms, and dispersed by the ants. This symbiosis evolved approximately 50-60 million years ago in the late Paleocene or early Eocene, and since its origin attine ants have acquired a variety of fungal mutualists in the Leucocoprineae and the distantly related Pterulaceae. The most specialized symbiotic interaction is referred to as "higher agriculture" and includes leafcutter ant agriculture in which the ants cultivate the single species Leucoagaricus gongylophorus. Higher agriculture fungal cultivars are characterized by specialized hyphal tip swellings, so-called gongylidia, which are considered a unique, derived morphological adaptation of higher attine fungi thought to be absent in lower attine fungi. Rare reports of gongylidia-like structures in fungus gardens of lower attines exist, but it was never tested whether these represent rare switches of lower attines to L. gonglyphorus cultivars or whether lower attine cultivars occasionally produce gongylidia. Here we describe the occurrence of gongylidia-like structures in fungus gardens of the asexual lower attine ant Mycocepurus smithii. To test whether M. smithii cultivates leafcutter ant fungi or whether lower attine cultivars produce gongylidia, we identified the M. smithii fungus utilizing molecular and morphological methods. Results shows that the gongylidia-like structures of M. smithii gardens are morphologically similar to gongylidia of higher attine fungus gardens and can only be distinguished by their slightly smaller size. A molecular phylogenetic analysis of the fungal ITS sequence indicates that the gongylidia-bearing M. smithii cultivar belongs to the so-called "Clade 1"of lower Attini cultivars. Given that M. smithii is capable of cultivating a morphologically and genetically diverse array of fungal symbionts, we discuss whether asexuality of the ant host maybe correlated with low partner fidelity and active symbiont choice between fungus and ant mutualists.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Agaricales / cytology
  • Agaricales / genetics
  • Agaricales / growth & development*
  • Animals
  • Ants / physiology*
  • Bayes Theorem
  • Behavior, Animal*
  • Likelihood Functions
  • Phylogeny
  • Reproduction, Asexual
  • Symbiosis

Grants and funding

FCP and MB are grateful to CNPq and Fapesp for their financial support. VEM is a recipient of a CAPES/PEC-PG scholarship. CR was financially supported by a Junior Fellowship from the Harvard Society of Fellows and the HMS Milton Fund. TS was supported by the U.S. National Science Foundation grant DEB 0949689, the Smithsonian Institution Scholarly Studies Program, and the Smithsonian NMNH Small Grants Program. HHDFL was supported by grants from the Danish Research Council and the Carlsberg Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.