Patterns of Specificity of the Pathogen <i>Escovopsis</i> across the Fungus-Growing Ant Symbiosis

Birnbaum, Stephanie S.L.

doi:10.1086/686911

Cited by 22 publications

(22 citation statements)

References 69 publications

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“…The specialized fungal parasites in the genus Escovopsis Muchovej and Della Lucia (Ascomycota: Hypocreales), which are found only in association with attine nests and which compete with the ants to feed on the fungal cultivars, are only partially known for species in these genera. To date, studies have focused on Escovopsis species associated with four Mycetomoellerius species [M. zeteki (Weber), M. ruthae (Weber), M. dichrous (Kempf), M. atlanticus (Mayhé-Nunes and Brandão)] and one Paratrachymyrmex species (P. diversus) (Currie et al, 1999a;Currie et al, 2003a;Meirelles et al, 2014Meirelles et al, , 2015Birnbaum & Gerardo, 2016).…”

Section: Speciesmentioning

confidence: 99%

“…Five distinct agricultural systems have been recognized. Each is broadly characterized by associations between phylogenetic groups (clades or grades) of ants and corresponding phylogenetic groups of fungi that are parasitized by phylogenetic groups of parasitic ascomycete fungi in the genus Escovopsis, as well as by the substrate upon which the fungi are cultivated (Weber, 1972;Gerardo et al, 2004Gerardo et al, , 2006Schultz & Brady, 2008;Mehdiabadi & Schultz, 2010;Meirelles et al, 2015;Birnbaum & Gerardo, 2016). Of these, undoubtedly the most celebrated are the 52 described species of leaf-cutting ants in the genera Acromyrmex Mayr and Atta Fabricius (Hölldobler & Wilson, 1990;Hölldobler & Wilson, 2011;Rabeling et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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The molecular phylogenetics ofTrachymyrmexForel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher‐attine’ ant agriculture

Solomon

Rabeling

Sosa‐Calvo

et al. 2019

Systematic Entomology

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The fungus‐growing ants and their fungal cultivars constitute a classic example of a mutualism that has led to complex coevolutionary dynamics spanning c. 55–65 Ma. Of the five agricultural systems practised by fungus‐growing ants, higher‐attine agriculture, of which leaf‐cutter agriculture is a derived subset, remains poorly understood despite its relevance to ecosystem function and human agriculture across the Neotropics and parts of North America. Among the ants practising higher‐attine agriculture, the genus Trachymyrmex Forel, as currently defined, shares most‐recent common ancestors with both the leaf‐cutter ants and the higher‐attine genera Sericomyrmex Mayr and Xerolitor Sosa‐Calvo et al. Although previous molecular‐phylogenetic studies have suggested that Trachymyrmex is a paraphyletic grade, until now insufficient taxon sampling has prevented a full investigation of the evolutionary history of this group and limited the possibility of resolving its taxonomy. Here we describe the results of phylogenetic analyses of 38 Trachymyrmex species, including 27 of the 49 described species and at least 11 new species, using four nuclear markers, as well as phylogenetic analyses of the fungi cultivated by 23 species of Trachymyrmex using two markers. We generated new genetic data for 112 ants (402 new gene sequences) and 95 fungi (153 new gene sequences). Our results corroborate previous findings that Trachymyrmex, as currently defined, is paraphyletic. We propose recognizing two new genera, Mycetomoellerius gen.n. and Paratrachymyrmex gen.n., and restricting the continued use of Trachymyrmex to the clade of nine largely North American species that contains the type species [Trachymyrmex septentrionalis (McCook)] and that is the sister group of the leaf‐cutting ants. Our fungal cultivar phylogeny generally corroborates previously observed broad patterns of ant–fungus association, but it also reveals further violations of those patterns. Higher‐attine fungi are divided into two groups: (i) the single species Leucoagaricus gongylophorus (Möller); and (ii) its sister clade, consisting of multiple species, recently referred to as Leucoagaricus Singer ‘clade B’. Our phylogeny indicates that, although most non‐leaf‐cutting higher‐attine ants typically cultivate species in clade B, some species cultivate L. gongylophorus, whereas still others cultivate fungi typically associated with lower‐attine agriculture. This indicates that the attine agricultural systems, which are currently defined by associations between ants and fungi, are not entirely congruent with ant and fungal phylogenies. They may, however, be correlated with as yet poorly understood biological traits of the ants and/or of their microbiomes.

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Section: Speciesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The molecular phylogenetics ofTrachymyrmexForel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher‐attine’ ant agriculture

Solomon

Rabeling

Sosa‐Calvo

et al. 2019

Systematic Entomology

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“…ants, like the strain genomically described here, are typically able to infect fungi cultivated by Atta and other leaf-cutting ant species but have narrow abilities to attack fungi grown by non-leaf-cutting ant species (60). In fact, even within a symbiosis involving a single ant species and its associated fungi, there can be variation in host range, suggesting genotypeby-genotype specificity (14,15,60). Therefore, the annotation of this first Escovopsis genome provides a starting point to investigate the genomic changes underlying a dynamically evolving host-pathogen system.…”

Section: Discussionmentioning

confidence: 94%

Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture

Man

Stajich

Kubicek

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite’s genome.

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“…Escovopsis presents wide morphological (different spore colors and other markers) and phylogenetic diversity, which is not entirely represented by the seven currently described species (Meirelles et al 2015a;Birnbaum and Gerardo 2016). Morphologically distinct Escovopsis species infect different fungal cultivars, suggesting patterns of specialization are shaped by co-evolutionary processes in this parasite-host interaction (Gerardo et al 2006;Birnbaum and Gerardo 2016). Escovopsis kreiselii (a pinkspored species) was isolated and described from colonies of the lower attine Mycetophylax morschi (Meirelles et al 2015b).…”

Section: Introductionmentioning

confidence: 99%

Escovopsis kreiselii specialization to its native hosts in the fungiculture of the lower attine ant Mycetophylax morschi

Custódio

Rodrigues

2018

Antonie van Leeuwenhoek

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Parasite-host associations are widespread in nature and the fungus-growing ants are considered model organisms to study such interactions. These insects cultivate basidiomycetous fungi for food, which are threatened by mycotrophic fungi in the genus Escovopsis. Although recently described from colonies of the lower attine ant Mycetophylax morschi, the biology and pathogenicity of Escovopsis kreiselii are unknown. Herein, we evaluated the interaction of E. kreiselii with fungi cultivated by M. morschi (native hosts) and with a fungus cultivated by another attine ant species (non-native host). In addition, we examined the physical interactions between hypha of E. kreiselii and hypha from its native hosts using scanning electron microscopy. Escovopsis kreiselii inhibited the growth of fungal cultivars by 24% or more (with exception of one isolate), when compared to the fungal cultivars growing alone. Escovopsis kreiselii is attracted towards its native hosts through chemotaxis and inhibition occurs when there is physical contact with the hyphae of the fungal cultivar. As reported for Escovopsis parasites associated with leafcutter ants (higher attines), E. kreiselii growth increased in the presence of its native hosts, even before contact between both fungi occurred. In interactions with the fungal cultivar that is not naturally infected by E. kreiselii (non-native host), it caused inhibition but not at the same magnitude as in native hosts. Multiple lines of evidence suggest that E. kreiselii is an antagonist of the fungus cultivated by M. morschi and can chemically recognize such fungus.

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Patterns of Specificity of the Pathogen Escovopsis across the Fungus-Growing Ant Symbiosis

Cited by 22 publications

References 69 publications

The molecular phylogenetics ofTrachymyrmexForel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher‐attine’ ant agriculture

The molecular phylogenetics ofTrachymyrmexForel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher‐attine’ ant agriculture

Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture

Escovopsis kreiselii specialization to its native hosts in the fungiculture of the lower attine ant Mycetophylax morschi

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