Cooperation, conflict, and coevolution in the attine ant-fungus symbiosis

Mehdiabadi, Natasha J.; Hughes, Benjamin; Mueller, Ulrich G.

doi:10.1093/beheco/arj028

Cited by 27 publications

(28 citation statements)

References 24 publications

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“…and that the origin of C. muelleri may have coincided with, or even have been driven by, a switch from the Clade 1 to Clade 2 cultivar 31 . The younger evolutionary age of Clade 2 relative to Clade 1 16 is consistent with this scenario, as is experimental work demonstrating that Clade 2-cultivating Panamanian C. muelleri ants accept the cultivar of C. longiscapus, whereas C. longiscapus ants do not readily accept the cultivar of C. muelleri 33,34 , reflecting an asymmetric ancestral/derived host-tolerance pattern also known from insect-plant coevolution 35 .…”

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confidence: 72%

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Symbiont fidelity and the origin of species in fungus-growing ants

et al. 2012

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A major problem in evolutionary biology is explaining the success of mutualism. solving this problem requires understanding the level of fidelity between interacting partners. Recent studies have proposed that fungus-growing ants and their fungal cultivars are the products of 'diffuse' coevolution, in which single ant and fungal species are not exclusive to one another. Here we show for ants and associated fungi in the Cyphomyrmex wheeleri species group that each ant species has been exclusively associated with a single fungal cultivar 'species' for millions of years, even though alternative cultivars are readily available, and that rare shifts to new cultivars are associated with ant speciation. such long-term partner fidelity may have facilitated 'tight' ant-fungus coevolution, and shifts to new fungal cultivars may have had a role in the origin of new ant species.

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confidence: 72%

“…1), even though nests of the two species occur in sympatry and, indeed, may be separated by only a few centimetres in some localities 12,26,[31][32][33] . Based on evidence from morphology and biogeography, it was previously hypothesized that C. muelleri may be derived from an ancestor resembling C. longiscapus s.l.…”

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Symbiont fidelity and the origin of species in fungus-growing ants

et al. 2012

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“…Partner fidelity feedback alone should impede the invasion of non-productive cultivar types into populations of A. texana , but a second mechanism, ant-mediated symbiont choice that biases cultivar propagation against inferior cultivar mutants, may also operate in the Atta ant-fungus mutualism [2], [51]. However, lab experiments quantifying symbiont choice in A. texana suggest that choice may be a comparatively weak mechanism, as workers do not show a strong and consistent cultivation-bias between closely-related Attamyces strains presented to the ants in laboratory experiments [22, R. Sen & U.G.…”

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confidence: 99%

Monoculture of Leafcutter Ant Gardens

et al. 2010

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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.

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“…The lower-attine subweb consists of at least two independently acquired cultivar clades (clades 1 and 2; Mueller et al 1998). Patterns of host use vary among lowerattine ant species, ranging from specialization to generality (Mueller et al 1998;Mehdiabadi et al 2006). The lower-attine cultivars are closely linked to free-living populations either because of repeated domestication or through frequent escape from the symbiosis; lower-attine cultivars have no known modifications for ant cultivation (Mueller et al 1998;Vo et al 2009).…”

Section: E127mentioning

confidence: 99%

Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

Mikheyev

Mueller

Abbot

2010

The American Naturalist

109

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: The mutualistic symbiosis between fungus-gardening ants and their cultivars has made fundamental contributions to our understanding of the coevolution of complex species interactions. Reciprocal specialization and vertical symbiont cotransmission are thought to promote a pattern of largely synchronous coevolutionary diversification in attines. Here we test this hypothesis by inferring the first time-calibrated multigene phylogeny of the lepiotaceous attine cultivars and comparing it with the recently published fossilanchored phylogeny of the attine ants. While this comparison reveals some possible cases of synchronous origins of ant and fungal clades, there were a number of surprising asynchronies. For example, leafcutter cultivars appear to be significantly younger than the corresponding ant genera. Similarly, a clade of fungi interacting with primitive fungus-gardening ants-thought to be ancestral to the more derived leaf-cutter symbionts-appears instead to be a more recent acquisition from free-living stock. These macroevolutionary patterns are consistent with recent population-level studies suggesting occasional acquisition of novel cultivar types from environmental sources and horizontal transmission of cultivars between different ant species. Horizontal transmission events, even if rare, appear to form loose ecological connections between diffusely coevolving ant and fungus lineages that permit punctuated changes in the topology of the mutualistic ant-fungus interaction network.

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Cooperation, conflict, and coevolution in the attine ant-fungus symbiosis

Cited by 27 publications

References 24 publications

Symbiont fidelity and the origin of species in fungus-growing ants

Symbiont fidelity and the origin of species in fungus-growing ants

Monoculture of Leafcutter Ant Gardens

Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

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