Rethinking crop-disease management in fungus-growing ants

Boomsma, Jacobus J.; Aanen, Duur K.

doi:10.1073/pnas.0910004106

Cited by 24 publications

(23 citation statements)

References 21 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The observed minor mutational variation in Atta gardens is significant, as any such variation at non-neutral loci provides the raw material for cultivar evolution, either through direct selection on the cultivar in cultivar-cultivar competition [20], [31], ant-mediated selection on the cultivar through symbiont choice (‘artificial selection’) [22], [31], [48], [49], or selection on ant-fungus combinations [31], [50].…”

Section: Discussionmentioning

confidence: 99%

Monoculture of Leafcutter Ant Gardens

et al. 2010

View full text Add to dashboard Cite

BackgroundLeafcutter ants depend on the cultivation of symbiotic Attamyces fungi for food, which are thought to be grown by the ants in single-strain, clonal monoculture throughout the hundreds to thousands of gardens within a leafcutter nest. Monoculture eliminates cultivar-cultivar competition that would select for competitive fungal traits that are detrimental to the ants, whereas polyculture of several fungi could increase nutritional diversity and disease resistance of genetically variable gardens.Methodology/Principal FindingsUsing three experimental approaches, we assessed cultivar diversity within nests of Atta leafcutter ants, which are most likely among all fungus-growing ants to cultivate distinct cultivar genotypes per nest because of the nests' enormous sizes (up to 5000 gardens) and extended lifespans (10–20 years). In Atta texana and in A. cephalotes, we resampled nests over a 5-year period to test for persistence of resident cultivar genotypes within each nest, and we tested for genetic differences between fungi from different nest sectors accessed through excavation. In A. texana, we also determined the number of Attamyces cells carried as a starter inoculum by a dispersing queens (minimally several thousand Attamyces cells), and we tested for genetic differences between Attamyces carried by sister queens dispersing from the same nest. Except for mutational variation arising during clonal Attamyces propagation, DNA fingerprinting revealed no evidence for fungal polyculture and no genotype turnover during the 5-year surveys.Conclusions/Significance Atta leafcutter ants can achieve stable, fungal monoculture over many years. Mutational variation emerging within an Attamyces monoculture could provide genetic diversity for symbiont choice (gardening biases of the ants favoring specific mutational variants), an analog of artificial selection.

show abstract

Section: Discussionmentioning

confidence: 99%

Monoculture of Leafcutter Ant Gardens

et al. 2010

View full text Add to dashboard Cite

show abstract

“…This has resulted in a steady flow of publications on the biology, ecology and molecular phylogeny of Escovopsis [22]–[33]; including ant defence strategies to control such mycoparasites [34]–[39]. Earlier, Currie et al [13], using morphological characters, had identified at least eight distinct taxa of Escovopsis from attine nests in Panama alone, but these have never been described, and publications since then have confirmed the high genetic diversity amongst isolates of Escovopsis from fungal gardens [23], [32].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

View full text Add to dashboard Cite

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.

show abstract

“…Because of a regrettable oversight, the original report did not specify the microbial methods for isolating Pseudonocardia from attine ants (Currie et al 1999b), and it was not until 2005, with the first publications of the exact methods to isolate Pseudonocardia from ants (Cafaro and Currie 2005), that other research groups began to evaluate the earlier findings. Reviewing the history of ant-actinomycete research in a recent commentary, Boomsma and Aanen (2009) concluded that there exists a need for more careful hypothesis testing to prevent oversimplified evolutionary conclusions, and that a key message from ten years of ant-Pseudonocardia research may be the reminder to scientists at large “to continuously re-evaluate what we know for a fact and what we merely infer”.…”

Section: Introductionmentioning

confidence: 99%

“…Following Boomsma and Aanen’s (2009) call for more careful hypothesis testing to avoid premature conclusions of adaptive and co-evolved antibiotic design (sensu Gould and Lewontin 1979), we expand here on a test of phylogenetic predictions that was first explored by Mueller et al (2008), testing for close phylogenetic affinities between ant-associated and environmental Pseudonocardia lineages. This same test can now be applied to a much larger dataset, because four times the sequence information has become available at GenBank for Pseudonocardia.…”

Section: Introductionmentioning

confidence: 99%

Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models

Mueller

Ishak

Lee

et al. 2010

Antonie van Leeuwenhoek

View full text Add to dashboard Cite

We reconstruct the phylogenetic relationships within the bacterial genus Pseudonocardia to evaluate two models explaining how and why Pseudonocardia bacteria colonize the microbial communities on the integument of fungus-gardening ant species (Attini, Formicidae). The traditional CoevolutionCodivergence model views the integument-colonizing Pseudonocardia as mutualistic microbes that are largely vertically transmitted between ant generations and that supply antibiotics that specifically suppress the garden pathogen Escovopsis. The more recent Acquisition model views Pseudonocardia as part of a larger integumental microbe community that frequently colonizes the ant integument from environmental sources (e.g., soil, plant material). Under this latter model, ant-associated Pseudonocardia may have diverse ecological roles on the ant integument (possibly ranging from pathogenic, to commensal, to mutualistic) and are not necessarily related to Escovopsis suppression. We test distinct predictions of these two models regarding the phylogenetic proximity of antassociated and environmental Pseudonocardia. We amassed 16S-rRNA gene sequence information for 87 attine-associated and 238 environmental Pseudonocardia, aligned the sequences with the help of RNA secondary structure modeling, and reconstructed phylogenetic relationships using a maximum-likelihood approach. We present 16S-rRNA secondary structure models of representative Pseudonocardia species to improve sequence alignments and identify sequencing errors. Our phylogenetic analyses reveal close affinities and even identical sequence matches between environmental Pseudonocardia and ant-associated Pseudonocardia, as well as nesting of Electronic supplementary material The online version of this article (doi:10.1007/s10482-010-9427-3) contains supplementary material, which is available to authorized users. environmental Pseudonocardia in subgroups that were previously thought to be specialized to associate only with attine ants. The great majority of ant associated Pseudonocardia are closely related to autotrophic Pseudonocardia and are placed in a large subgroup of Pseudonocardia that is known essentially only from cultured isolates (rather than cloned 16S sequences). The preponderance of the known ant-associated Pseudonocardia in this latter clade of culturable lineages may not necessarily reflect abundance of these Pseudonocardia types on the ants, but isolation biases when screening for Pseudonocardia (e.g., preferential isolation of autotrophic Pseudonocardia with minimum-nutrient media). The accumulated phylogenetic patterns and the possibility of isolation biases in previous work further erode support for the traditional Coevolution-Codivergence model and calls for continued revision of our understanding how and why Pseudonocardia colonize the microbial communities on the integument of fungus-gardening ant species. NIH Public Access

show abstract

Rethinking crop-disease management in fungus-growing ants

Cited by 24 publications

References 21 publications

Monoculture of Leafcutter Ant Gardens

Monoculture of Leafcutter Ant Gardens

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

Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models

Contact Info

Product

Resources

About