Yet More “Weeds” in the Garden: Fungal Novelties from Nests of Leaf-Cutting Ants

Abstract

BackgroundSymbiotic relationships modulate the evolution of living organisms in all levels of biological organization. A notable example of symbiosis is that of attine ants (Attini; Formicidae: Hymenoptera) and their fungal cultivars (Lepiotaceae and Pterulaceae; Agaricales: Basidiomycota). In recent years, this mutualism has emerged as a model system for studying coevolution, speciation, and multitrophic interactions. Ubiquitous in this ant-fungal symbiosis is the “weedy” fungus Escovopsis (Hypocreales: Ascomycota), known only as a mycoparasite of attine fungal gardens. Despite interest in its biology, ecology and molecular phylogeny—noting, especially, the high genetic diversity encountered—which has led to a steady flow of publications over the past decade, only two species of Escovopsis have formally been described.Methods and ResultsWe sampled from fungal gardens and garden waste (middens) of nests of the leaf-cutting ant genus Acromyrmex in a remnant of subtropical Atlantic rainforest in Minas Gerais, Brazil. In culture, distinct morphotypes of Escovopsis sensu lato were recognized. Using both morphological and molecular analyses, three new species of Escovopsis were identified. These are described and illustrated herein—E. lentecrescens, E. microspora, and E. moelleri—together with a re-description of the genus and the type species, E. weberi. The new genus Escovopsioides is erected for a fourth morphotype. We identify, for the first time, a mechanism for horizontal transmission via middens.ConclusionsThe present study makes a start at assigning names and formal descriptions to these specific fungal parasites of attine nests. Based on the results of this exploratory and geographically-restricted survey, we expect there to be many more species of the genus Escovopsis and its relatives associated with nests of both the lower and higher Attini throughout their neotropical range, as suggested in previous studies.

Towards a natural classification and backbone tree for Sordariomycetes

“…In culture it produces a brush-like asexual morph with phialides on well-defined vesicles in culture. It differs from Escovopsis by the absence of pigmentation, the lageniform phialides produced on terminal and intercalary, globose vesicles, the hyaline, smooth conidia in long chains, as well as sequence data (Augustin et al 2013). According to the phylogenetic analyses of ITS and LSU sequence data this genus belongs in Hypocreaceae.…”

Unraveling Trichoderma species in the attine ant environment: description of three new taxa

“…However, studies focused on the taxonomy and systematics of filamentous fungi associated with these insects have only considered the genus Escovopsis, the specialized parasite of the mutualistic fungus (Currie et al 1999;Currie et al 2003;Muchovej and Della Lucia 1990;Seifert et al 1995;Augustin et al 2013;Masiulionis et al 2015;Meirelles et al 2015). These studies showed the presence of several new Escovopsis species, which suggests that attine ants colonies might also harbor a high diversity of filamentous fungi, including potential new species of the genus…”

Quality control by leaf-cutting ants: evidence from communities of endophytic fungi in foraged and rejected vegetation

“…This pattern was also repeated with Phomopsis, although some species of the genus are known to produce compounds toxic to insects (Webber 1981), as well as to fungi (Wijeratne et al 2006;Huang et al 2008;Borges et al 2009). An intriguing possibility is that the ants actively prefer material with antifungal properties-if this activity does not affect the basidiomycete mutualist Leucoagaricus but does inhibit ascomycete parasites such as Escovopsis (Augustin et al 2013), then the ants could effectively be medicating their fungal symbiont. Some species of Xylaria are producers of toxins that can have negative effects on both insects (Azevedo et al 2000) and fungi (Boonphong et al 2001), but based on our results, it seems that Xylaria does not represent a threat to the ants or to the fungal symbiont.…”