Specific, non-nutritional association between an ascomycete fungus and Allomerus plant-ants

Abstract

Ant -fungus associations are well known from attine ants, whose nutrition is based on a symbiosis with basidiomycete fungi. Otherwise, only a few non-nutritional ant -fungus associations have been recorded to date. Here we focus on one of these associations involving Allomerus plant-ants that build galleried structures on their myrmecophytic hosts in order to ambush prey. We show that this association is not opportunistic because the ants select from a monophyletic group of closely related fungal haplotypes of an ascomycete species from the order Chaetothyriales that consistently grows on and has been isolated from the galleries. Both the ants' behaviour and an analysis of the genetic population structure of the ants and the fungus argue for host specificity in this interaction. The ants' behaviour reveals a major investment in manipulating, growing and cleaning the fungus. A molecular analysis of the fungus demonstrates the widespread occurrence of one haplotype and many other haplotypes with a lower occurrence, as well as significant variation in the presence of these fungal haplotypes between areas and ant species. Altogether, these results suggest that such an interaction might represent an as-yet undescribed type of specific association between ants and fungus in which the ants cultivate fungal mycelia to strengthen their hunting galleries.

Trade-offs in an ant–plant–fungus mutualism

“…In ant-plant interactions, the protection of plants by ants is most often the indirect result of foraging and territorial activities on host leaves, which are by-products of the 'selfish' activities of the colonies [11,42]. Allomerus species have developed an alternative to this classic foraging behaviour, thanks to an investment in the construction of galleries they use to ambush prey and, in the species studied thus far, the galleries are reinforced by the mycelium of a specific fungus [21,22]. The differences in investment in gallery construction (and thus fungal cultivation) and in the use of the galleries induce variations in the outcomes experienced by the host plant.…”

“…Plant identification was confirmed by M.-F. Prévost after comparison with voucher specimens deposited at the Cayenne Herbarium (http:// publish.plantnet-project.org/project/caypub), the ants were identified by J.H.C. Delabie at the Laboratorio de Mirmecologia, Cocoa Research Centre, Ilhéus, Bahia, Brazil where voucher specimens were deposited and the ITS-EF1a DNA sequences of the fungal haplotypes are accessible from GenBank (see [21]). …”

“…These two ant species also cultivate a specific fungus, Trimmatostroma sp. (Chaetothyriales), that they use to build galleries under the stems of their host plant to capture prey [21,22]. By interacting with plant tissues, the fungus also improves nutrient uptake by the host plant [23].…”

A phylogenetic perspective on the association between ants (Hymenoptera: Formicidae) and black yeasts (Ascomycota: Chaetothyriales)

“…Ant-associated Chaetothyriales can be classified into three main functional groups: (i) strains associated with fungus-growing attine ants [10][11][12]; (ii) strains involved in 'carton' structures built by ants [7,[13][14][15]; and (iii) strains associated with ant-plant symbioses [7,16]. The first group, Chaetothyriales associated with attine ants, are not the focus of our study.…”

“…Botryosphaeriales, Eurotiales, Capnodiales, Chaetothyriales, Hypocreales, Pleosporales) can be isolated from carton. Only strains of the orders Chaetothyriales and Capnodiales are isolated from pieces of hyphae and are thus considered to have a structural function in carton construction [7,[13][14][15]. The other strains have been isolated only from spores and are most likely contaminants.…”