Coevolution between attine ants and actinomycete bacteria: A reevaluation

Ulrich G. Mueller, Debadutta Dash, Christian Rabeling, Andre Rodrigues

Research output: Contribution to journalArticle

97 Citations (Scopus)

Abstract

We reassess the coevolution between actinomycete bacteria and fungus-gardening (attine) ants. Actinomycete bacteria are of special interest because they are metabolic mutualists of diverse organisms (e.g., in nitrogen-fixation or antibiotic production) and because Pseudonocardia actinomycetes are thought to serve disease-suppressing functions in attine gardens. Phylogenetic information from culture-dependent and culture-independent microbial surveys reveals (1) close affinities between free-living and ant-associated Pseudonocardia, and (2) essentially no topological correspondence between ant and Pseudonocardia phylogenies, indicating frequent bacterial acquisition from environmental sources. Identity of ant-associated Pseudonocardia and isolates from soil and plants implicates these environments as sources from which attine ants acquire Pseudonocardia. Close relatives of Atta leafcutter ants have abundant Pseudonocardia, but Pseudonocardia in Atta is rare and appears at the level of environmental contamination. In contrast, actinomycete bacteria in the genera Mycobacterium and Microbacterium can be readily isolated from gardens and starter-cultures of Atta. The accumulated phylogenetic evidence is inconsistent with prevailing views of specific coevolution between Pseudonocardia, attine ants, and garden diseases. Because of frequent acquisition, current models of Pseudonocardia-disease coevolution now need to be revised. The effectiveness of Pseudonocardia antibiotics may not derive from advantages in the coevolutionary arms race with specialized garden diseases, as currently believed, but from frequent recruitment of effective microbes from environmental sources. Indeed, the exposed integumental structures that support actinomycete growth on attine ants argue for a morphological design facilitating bacterial recruitment. We review the accumulated evidence that attine ants have undergone modifications in association with actinomycete bacteria, but we find insufficient support for the reverse, modifications of the bacteria resulting from the interaction with attine ants. The defining feature of coevolution - reciprocal modification - therefore remains to be established for the attine ant-actinomycete mutualism.

Original languageEnglish (US)
Pages (from-to)2894-2912
Number of pages19
JournalEvolution
Volume62
Issue number11
DOIs
StatePublished - Nov 1 2008
Externally publishedYes

Fingerprint

Pseudonocardia
Ants
Actinobacteria
coevolution
ant
Formicidae
Bacteria
bacterium
bacteria
Atta
gardens
garden
antibiotics
phylogeny
Gardening
Microbacterium
Anti-Bacterial Agents
phylogenetics
arms race
beneficial microorganisms

Keywords

  • Atta
  • Attini
  • Fungus-growing ants
  • Mutualism
  • Pseudonocardia
  • Symbiosis

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

Cite this

Coevolution between attine ants and actinomycete bacteria : A reevaluation. / Mueller, Ulrich G.; Dash, Debadutta; Rabeling, Christian; Rodrigues, Andre.

In: Evolution, Vol. 62, No. 11, 01.11.2008, p. 2894-2912.

Research output: Contribution to journalArticle

Mueller, Ulrich G. ; Dash, Debadutta ; Rabeling, Christian ; Rodrigues, Andre. / Coevolution between attine ants and actinomycete bacteria : A reevaluation. In: Evolution. 2008 ; Vol. 62, No. 11. pp. 2894-2912.
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