Repeated Evolution of Fungal Cultivar Specificity in Independently Evolved Ant-Plant-Fungus Symbioses

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.

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

“…In addition, a recently described species, Arthrocladium tardum (Trichomeriaceae), has been isolated both from a domatium of Leonardoxa africana occupied by the ant Petalomyrmex phylax in Cameroon and from decaying coconut shells in Brazil [6]. Although some Chaetothyriales strains are clearly mutualistic symbionts of ants [28,33,34], our study indicates that ant nests can be colonized by opportunistic species and that Chaetothyriales taxa might display exceptional dispersal capacities and surprising ubiquity. In the future, it will be most useful to investigate the degree of specialization of the interactions between particular ant and fungal partners in order to interpret the phylogenetic pattern in evolutionary terms.…”

“…africana, Tetraponera aethiops on Barteria fistulosa and Crematogaster margaritae on Keetia hispida. We found that each ant-plant symbiosis had its own set of domatia fungal strains [7,28]. In Central America, four Azteca species living with three different Cecropia species were investigated along a transect of a few kilometres length.…”

Impact of primer choice on characterization of orchid mycorrhizal communities using 454 pyrosequencing

“…; Blatrix et al . ). Sequences were clustered into OTUs using the average neighbour method and default MOTHUR settings.…”

Protection against herbivory in the mutualism between Pseudomyrmex dendroicus (Formicidae) and Triplaris americana (Polygonaceae)

“…Although these plants produce no food bodies or extrafloral nectaries, rewards to the ants are provided by a third symbiont -scale insects (Coccoidea, Hemiptera) in the form of honeydew (Schremmer 1984, Davidson and McKey 1993, Ward 1999. It has also been suggested that another symbiont -fungi is involved and may also provide food (Schremmer 1984, Defossez et al 2009, Blatrix et al 2013. Pseudomyrmex (Formicidae, Pseudomyrmecinae) is a genus that comprises ca.…”