Instability of novel ant-fungal associations constrains horizontal exchange of fungal symbionts

• Published in: Evolutionary ecology Vol. 28; no. 1; pp. 157 - 176
• Main Authors: Seal, Jon N., Mueller, U. G.
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 2014; Springer; Springer Nature B.V
• Subjects: Animal Ecology; Ants; Attini; Biomedical and Life Sciences; Cultivars; Ecology; Evolution; Evolutionary Biology; Formicidae; Fungi; Gardens; Gardens & gardening; Immunology; Life Sciences; Original Paper; Physiological aspects; Plant Sciences; Symbiosis; Trachymyrmex; Attini; Fungi; Symbiosis; Disease; Coevolution; Immunity; Colony performance
• ISSN: 0269-7653; 1573-8477
• DOI: 10.1007/s10682-013-9665-8

One of the more fascinating features of fungus-gardening ants (Attini: Formicidae) is their fidelity to their lineage-specific fungal symbionts. Among the derived higher-attine ants (leafcutter ants and close relatives), it is thought that most leaf-cutting ants grow
Attamyces
fungus whereas most
Trachymyrmex
ants grow ‘Trachymyces’ fungus, but there exist exceptions to this clade-to-clade correspondence between ants and fungi. The exceptions are inconsistent with strict one-to-one coevolution, which suggests that ants sometimes are able to switch to novel fungi. Such switches appear to be largely constrained and ants are generally faithful to their species-specific fungi. Prior experiments demonstrated no clear fitness consequences of growing novel fungi over the short-term when the ant
Trachymyrmex septentrionalis
was symbiont-switched by forcing it to grow
Attamyces
leaf-cutter fungus. We hypothesized that long-term ant-fungal fidelity is constrained either by physiological differences among fungal species or by garden diseases that symbiont-switched ants cannot control. Repeat experiments in a different location show that
T. septentrionalis
colonies switched to grow
Attamyces
exhibit sudden declines in garden biomass and consequent fitness reductions due to garden destruction by pathogens, whereas control colonies (
Trachymyrmex
ants cultivating Trachymyces fungus) do not show parallel garden declines. These patterns are mirrored in symbiont-switch experiments conducted on colonies in
Trachymyrmex turrifex
. Disease microbes selecting on ant-cultivar combinations therefore can constrain switches to novel cultivars and maintain combinations that are more resistant to disease.