Repeated evolution of fungal cultivar specificity in independently evolved ant-plant-fungus symbioses

PLoS One. 2013 Jul 25;8(7):e68101. doi: 10.1371/journal.pone.0068101. Print 2013.

Abstract

Some tropical plant species possess hollow structures (domatia) occupied by ants that protect the plant and in some cases also provide it with nutrients. Most plant-ants tend patches of chaetothyrialean fungi within domatia. In a few systems it has been shown that the ants manure the fungal patches and use them as a food source, indicating agricultural practices. However, the identity of these fungi has been investigated only in a few samples. To examine the specificity and constancy of ant-plant-fungus interactions we characterised the content of fungal patches in an extensive sampling of three ant-plant symbioses (Petalomyrmex phylax/Leonardoxa africana subsp. africana, Aphomomyrmex afer/Leonardoxa africana subsp. letouzeyi and Tetraponera aethiops/Barteria fistulosa) by sequencing the Internal Transcribed Spacers of ribosomal DNA. For each system the content of fungal patches was constant over individuals and populations. Each symbiosis was associated with a specific, dominant, primary fungal taxon, and to a lesser extent, with one or two specific secondary taxa, all of the order Chaetothyriales. A single fungal patch sometimes contained both a primary and a secondary taxon. In one system, two founding queens were found with the primary fungal taxon only, one that was shown in a previous study to be consumed preferentially. Because the different ant-plant symbioses studied have evolved independently, the high specificity and constancy we observed in the composition of the fungal patches have evolved repeatedly. Specificity and constancy also characterize other cases of agriculture by insects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Africa
  • Animals
  • Ants / physiology*
  • Ascomycota / classification
  • Ascomycota / genetics*
  • Ascomycota / isolation & purification
  • Biological Evolution*
  • DNA, Fungal / classification
  • DNA, Fungal / genetics*
  • DNA, Intergenic / classification
  • DNA, Intergenic / genetics*
  • DNA, Ribosomal / classification
  • DNA, Ribosomal / genetics*
  • Fabaceae / physiology*
  • Phylogeny
  • Phylogeography
  • Symbiosis / physiology

Substances

  • DNA, Fungal
  • DNA, Intergenic
  • DNA, Ribosomal

Grants and funding

This project was supported by the network “Bibliothèque du Vivant” (http://bdv.ups-tlse.fr/), funded by the CNRS, the Muséum National d'Histoire Naturelle, the INRA and the CEA (Centre National de Séquençage). It was also funded by grants to R. Blatrix and D. McKey from three programmes of the French Agence Nationale de la Recherche (www.agence-nationale-recherche.fr): “Young scientists” (research agreement no. ANR-06-JCJC-0127), “Biodiversity” (IFORA project) and “Sixth extinction” (C3A project). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.