Abstract
Fungus-gardening (attine) ants grow fungus for food in protected gardens, which contain beneficial, auxiliary microbes, but also microbes harmful to gardens. Among these potentially pathogenic microorganisms, the most consistently isolated are fungi in the genus Escovopsis, which are thought to co-evolve with ants and their cultivar in a tripartite model. To test clade-to-clade correspondence between Escovopsis and ants in the higher attine symbiosis (including leaf-cutting and non-leaf-cutting ants), we amassed a geographically comprehensive collection of Escovopsis from Mexico to southern Brazil, and reconstructed the corresponding Escovopsis phylogeny. Contrary to previous analyses reporting phylogenetic divergence between Escovopsis from leafcutters and Trachymyrmex ants (non-leafcutter), we found no evidence for such specialization; rather, gardens from leafcutters and non-leafcutters genera can sometimes be infected by closely related strains of Escovopsis, suggesting switches at higher phylogenetic levels than previously reported within the higher attine symbiosis. Analyses identified rare Escovopsis strains that might represent biogeographically restricted endemic species. Phylogenetic patterns correspond to morphological variation of vesicle type (hyphal structures supporting spore-bearing cells), separating Escovopsis with phylogenetically derived cylindrical vesicles from ancestral Escovopsis with globose vesicles. The new phylogenetic insights provide an improved basis for future taxonomic and ecological studies of Escovopsis.
Highlights
Symbiotic relationships are a significant source for evolutionary innovation [1,2,3], generating diversity in mutualistic and parasitic interactions, among microbe–insect associations
Analysing Escovopsis strains isolated from 70 higher attine colonies (26 Atta colonies, 25 Acromyrmex, 18 Trachymyrmex, one Sericomyrmex), from at least 20 ant species in 31 locations, we show that leafcutter ants and other higher attine ants can share similar Escovopsis parasites, indicating no strict ant-parasite co-cladogenesis within this group of ants
12 of the 75 Escovopsis strains (16%) isolated from higher attine ants did not follow this pattern. These results show that Escovopsis infecting leaf-cutting ants and those infecting other higher attine ants are not reciprocally monophyletic, suggesting that these insects can share infections 6 caused by closely related strains of the parasite
Summary
Symbiotic relationships are a significant source for evolutionary innovation [1,2,3], generating diversity in mutualistic and parasitic interactions, among microbe–insect associations. During the last decades, understanding of microbe–insect interactions has significantly improved, revealing more complex interactions among an increasingly diverse set of participants than was previously appreciated. This is especially true for attine ants and their microbial symbionts, which have become among the best-studied examples for parasitic and mutualistic insect–microbe coevolution [4,5]. Higher attine ants cultivate phylogenetically derived fungi that exhibit hyphal swellings, called gongylidia, which are specialized structures used to feed the queen and the brood [11,12,13]
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