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Ulrich G. Mueller - One of the best experts on this subject based on the ideXlab platform.
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Landscape genomics of an obligate mutualism: Concordant and discordant population structures between the leafcutter ant Atta texana and its two main fungal symbiont types
Molecular ecology, 2019Co-Authors: Chad C. Smith, Jon N. Seal, Jesse N. Weber, Alexander S. Mikheyev, Flavio Roces, Martin Bollazzi, Katrin Kellner, Ulrich G. MuellerAbstract:To explore landscape genomics at the range limit of an obligate mutualism, we use genotyping-by-sequencing (ddRADseq) to quantify population structure and the effect of host-symbiont interactions between the northernmost fungus-farming leafcutter ant Atta texana and its two main types of cultivated fungus. Genome-wide differentiation between ants associated with either of the two fungal types is of the same order of magnitude as differentiation associated with temperature and precipitation across the ant's entire range, suggesting that specific ant-fungus genome-genome combinations may have been favoured by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. This population-genetic structure was concordant between the ants and one cultivar type (M-fungi, concordant clines) but discordant for the other cultivar type (T-fungi). Discordance in population-genetic structures between ant hosts and a fungal symbiont is surprising because the ant farmers codisperse with their vertically transmitted fungal symbionts. Discordance implies that (a) the fungi disperse also through between-nest horizontal transfer or other unknown mechanisms, and (b) genetic drift and gene flow can differ in magnitude between each partner and between different ant-fungus combinations. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome-genome interactions between host and symbiont influence adaptive genetic differentiation of the host during range evolution in this obligate mutualism.
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Landscape genomics of an obligate mutualism: discordant population structures between a leafcutter-ant and its fungal cultivars
2018Co-Authors: Chad C. Smith, Jon N. Seal, Jesse N. Weber, Alexander S. Mikheyev, Flavio Roces, Martin Bollazzi, Katrin Kellner, Ulrich G. MuellerAbstract:To explore landscape genomics at the range limit of an obligate mutualism, we used genotyping-by-sequencing (ddRADseq) to quantify population structure and the effect of host-symbiont interactions between the northernmost fungus-farming leafcutter ant Atta texana and its two main types of cultivated fungus. At local scales, genome-wide differentiation between ants associated with either of the two fungal types is greater than the differentiation associated with the abiotic factors temperature and precipitation, suggesting that specific ant-fungus genome-genome combinations may have been favored by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. In contrast, genetic structure was patchy in the cultivated fungi, with no consistent reduction of fungal genetic diversity at the range margins. This discordance in population-genetic structure between ant hosts and fungal symbionts is surprising because the ant farmers co-disperse with their vertically-transmitted fungal symbionts, but apparently the fungi disperse occasionally also through between-nest horizontal transfer or other unknown dispersal mechanisms. The discordance in population-genetic structure indicates that genetic drift and gene flow differ in magnitude between each partner in this leafcutter mutualism. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome-genome interactions between host and symbiont influences adaptive genetic differentiation of the host during range evolution in this obligate mutualism.
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Effects of substrate, ant and fungal species on plant fiber degradation in a fungus-gardening ant symbiosis
Journal of insect physiology, 2017Co-Authors: Alexandria M. Demilto, Ulrich G. Mueller, Katrin Kellner, Monte Rouquette, Jon N. SealAbstract:Abstract Fungus-gardening or attine ants have outsourced most of their digestive function to a symbiotic fungus. The ants feed their fungus – essentially an external digestive organ – a variety of substrates of botanical origin, including fresh and dried flowers, leaves and insect frass (processed leaves). Although plant tissues are rich in fibers (lignocelluloses, hemicelluloses, pectins and starches) and the symbiotic fungus possesses the genetic and enzymatic machinery to metabolize these compounds, the highly derived attines, the leaf-cutters ( Atta and Acromyrmex ), are known to produce fiber-rich waste. While leaf-cutting ants are important consumers of primary plant tissue, there have been fewer studies on physiological activity of fungi grown by closely related ant species in the genus Trachymyrmex , which generally grow related species of fungi, have smaller colonies and consume a wider variety of fungal substrates in addition to fresh leaves and flowers. In this study, we measured the cellulase activity of the fungus-gardening ants Atta texana , Trachymyrmex arizonensis and T. septentrionalis . We then quantified fiber consumption of the fungus-gardening ants Trachymyrmex septentrionalis and Trachymyrmex arizonensis by comparing the amounts and percentages present in their food and in fungus garden refuse during a controlled feeding experiment over the span of several months. Finally, we compared waste composition of T. arizonensis colonies growing different fungal strains, because this species is known to cultivate multiple strains of Leucoagaricus in its native range. The leaf-cutting ant A. texana was found to have lower cellulytic activity than T. arizonensis or T. septentrionalis . Total lignocellulose and hemicellulose amounts were significantly lower in refuse piles than in the substrates fed to the Trachymyrmex colonies, thus these fibers were consumed by the fungal symbionts of these ant species. Although lignocellulose utilization was similar in two distinct fungal species grown by T. arizonensis colonies, hemicellulose utilization was higher in T. arizonensis colonies growing a derived leaf-cutting ant fungal symbiont than when growing a native type of symbiont. The results of this study demonstrate that fiber digestion in fungus-gardening ants is an outcome of ant-fungal interaction.
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Dispersal of Attaphila fungicola , a symbiotic cockroach of leaf-cutter ants
Insectes Sociaux, 2017Co-Authors: Z. I. Phillips, M. M. Zhang, Ulrich G. MuellerAbstract:The myrmecophile cockroach Attaphila fungicola lives in the nests of leaf-cutter ants (Atta texana and A. cephalotes) and uses the female winged reproductives (i.e., female alates) of its host as vectors for the first phase of its dispersal. It is unknown whether A. fungicola remain with vectoring A. texana females after mating flights and throughout A. texana nest founding and subsequent colony development, or if the symbiotic cockroaches disperse to established A. texana colonies, either on their own or while still Attached to vectoring A. texana females. We captured A. fungicola Attached to A. texana female alates as they prepared for mating flights and measured their survivorship in artificial brood chambers with de-alate, recently mated A. texana queens and their incipient gardens, and in a non-natal established fungal garden tended by A. texana workers. After 13 days, 100% of A. fungicola had died in brood chambers with queens, while 100% of A. fungicola remained alive in the fungal garden chamber. We tested the feasibility of alternative modes of dispersal to established colonies by placing A. fungicola Attached and unAttached to vectoring female alates in the proximity of an established A. texana colony directly after a mating flight, and recorded whether A. fungicola entered the non-natal nest. A significantly higher proportion of A. fungicola Attached to vectoring alates entered the nest compared to unAttached A. fungicola. We also placed A. fungicola Attached to vectoring alates in a foraging chamber of a laboratory colony to determine if, once in the nest, A. fungicola could navigate to the fungal garden chamber; 100% of A. fungicola detached from their vectoring alates and entered the fungal garden chamber. We tested alate preference of A. fungicola by placing A. fungicola separately in containers with one A. texana female alate and one male alate; after 2 h, 71% of A. fungicola were Attached to female alates and 0% to male alates. Finally, we report the first record of a male A. fungicola collected during a mating flight of A. texana. These observations accumulated from field and laboratory studies suggest that A. fungicola vectored by A. texana female alates may not remain with foundresses, but instead disperse between established colonies through one or more alternative mechanisms. This study helps elucidate a tripartite ant-fungus-cockroach interaction, and provides a foundation for future research on Attaphila dispersal and reproductive biology.
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Bacterial microbiomes from vertically transmitted fungal inocula of the leaf-cutting ant Atta texana.
Environmental Microbiology Reports, 2016Co-Authors: Lucas A. Meirelles, Quinn S. Mcfrederick, Andre Rodrigues, Joana D. Mantovani, Cynara De Melo Rodovalho, Henrique Ferreira, Maurício Bacci, Ulrich G. MuellerAbstract:Microbiome surveys provide clues for the functional roles of symbiotic microbial communities and their hosts. In this study, we elucidated bacterial microbiomes associated with the vertically transmitted fungal inocula (pellets) used by foundress queens of the leaf-cutting ant Atta texana as starter-cultures for new gardens. As reference microbiomes, we also surveyed bacterial microbiomes of foundress queens, gardens and brood of incipient nests. Pseudomonas, Acinetobacter, Propionibacterium and Corynebacterium were consistently present in high abundance in microbiomes. Some pellet and ant samples contained abundant bacteria from an Entomoplasmatales-clade, and a separate PCR-based survey of Entomoplasmatales bacteria in eight attine ant-genera from Brazil placed these bacteria in a monophyletic clade within the bacterial genus Mesoplasma. The attine ant-Mesoplasma association parallels a similar association between a closely related, monophyletic Entomoplasmatales-clade and army ants. Of thirteen A. texana nests surveyed, three nests with exceptionally high Mesoplasma abundance died, whereas the other nests survived. It is unclear whether Mesoplasma was the primary cause of mortality, or Mesoplasma became abundant in moribund nests for non-pathogenic reasons. However, the consistent and geographically widespread presence of Mesoplasma suggests an important functional role in the association with attine ants.
Jon N. Seal - One of the best experts on this subject based on the ideXlab platform.
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Landscape genomics of an obligate mutualism: Concordant and discordant population structures between the leafcutter ant Atta texana and its two main fungal symbiont types
Molecular ecology, 2019Co-Authors: Chad C. Smith, Jon N. Seal, Jesse N. Weber, Alexander S. Mikheyev, Flavio Roces, Martin Bollazzi, Katrin Kellner, Ulrich G. MuellerAbstract:To explore landscape genomics at the range limit of an obligate mutualism, we use genotyping-by-sequencing (ddRADseq) to quantify population structure and the effect of host-symbiont interactions between the northernmost fungus-farming leafcutter ant Atta texana and its two main types of cultivated fungus. Genome-wide differentiation between ants associated with either of the two fungal types is of the same order of magnitude as differentiation associated with temperature and precipitation across the ant's entire range, suggesting that specific ant-fungus genome-genome combinations may have been favoured by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. This population-genetic structure was concordant between the ants and one cultivar type (M-fungi, concordant clines) but discordant for the other cultivar type (T-fungi). Discordance in population-genetic structures between ant hosts and a fungal symbiont is surprising because the ant farmers codisperse with their vertically transmitted fungal symbionts. Discordance implies that (a) the fungi disperse also through between-nest horizontal transfer or other unknown mechanisms, and (b) genetic drift and gene flow can differ in magnitude between each partner and between different ant-fungus combinations. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome-genome interactions between host and symbiont influence adaptive genetic differentiation of the host during range evolution in this obligate mutualism.
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Landscape genomics of an obligate mutualism: discordant population structures between a leafcutter-ant and its fungal cultivars
2018Co-Authors: Chad C. Smith, Jon N. Seal, Jesse N. Weber, Alexander S. Mikheyev, Flavio Roces, Martin Bollazzi, Katrin Kellner, Ulrich G. MuellerAbstract:To explore landscape genomics at the range limit of an obligate mutualism, we used genotyping-by-sequencing (ddRADseq) to quantify population structure and the effect of host-symbiont interactions between the northernmost fungus-farming leafcutter ant Atta texana and its two main types of cultivated fungus. At local scales, genome-wide differentiation between ants associated with either of the two fungal types is greater than the differentiation associated with the abiotic factors temperature and precipitation, suggesting that specific ant-fungus genome-genome combinations may have been favored by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. In contrast, genetic structure was patchy in the cultivated fungi, with no consistent reduction of fungal genetic diversity at the range margins. This discordance in population-genetic structure between ant hosts and fungal symbionts is surprising because the ant farmers co-disperse with their vertically-transmitted fungal symbionts, but apparently the fungi disperse occasionally also through between-nest horizontal transfer or other unknown dispersal mechanisms. The discordance in population-genetic structure indicates that genetic drift and gene flow differ in magnitude between each partner in this leafcutter mutualism. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome-genome interactions between host and symbiont influences adaptive genetic differentiation of the host during range evolution in this obligate mutualism.
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Effects of substrate, ant and fungal species on plant fiber degradation in a fungus-gardening ant symbiosis
Journal of insect physiology, 2017Co-Authors: Alexandria M. Demilto, Ulrich G. Mueller, Katrin Kellner, Monte Rouquette, Jon N. SealAbstract:Abstract Fungus-gardening or attine ants have outsourced most of their digestive function to a symbiotic fungus. The ants feed their fungus – essentially an external digestive organ – a variety of substrates of botanical origin, including fresh and dried flowers, leaves and insect frass (processed leaves). Although plant tissues are rich in fibers (lignocelluloses, hemicelluloses, pectins and starches) and the symbiotic fungus possesses the genetic and enzymatic machinery to metabolize these compounds, the highly derived attines, the leaf-cutters ( Atta and Acromyrmex ), are known to produce fiber-rich waste. While leaf-cutting ants are important consumers of primary plant tissue, there have been fewer studies on physiological activity of fungi grown by closely related ant species in the genus Trachymyrmex , which generally grow related species of fungi, have smaller colonies and consume a wider variety of fungal substrates in addition to fresh leaves and flowers. In this study, we measured the cellulase activity of the fungus-gardening ants Atta texana , Trachymyrmex arizonensis and T. septentrionalis . We then quantified fiber consumption of the fungus-gardening ants Trachymyrmex septentrionalis and Trachymyrmex arizonensis by comparing the amounts and percentages present in their food and in fungus garden refuse during a controlled feeding experiment over the span of several months. Finally, we compared waste composition of T. arizonensis colonies growing different fungal strains, because this species is known to cultivate multiple strains of Leucoagaricus in its native range. The leaf-cutting ant A. texana was found to have lower cellulytic activity than T. arizonensis or T. septentrionalis . Total lignocellulose and hemicellulose amounts were significantly lower in refuse piles than in the substrates fed to the Trachymyrmex colonies, thus these fibers were consumed by the fungal symbionts of these ant species. Although lignocellulose utilization was similar in two distinct fungal species grown by T. arizonensis colonies, hemicellulose utilization was higher in T. arizonensis colonies growing a derived leaf-cutting ant fungal symbiont than when growing a native type of symbiont. The results of this study demonstrate that fiber digestion in fungus-gardening ants is an outcome of ant-fungal interaction.
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Ant-fungus species combinations engineer physiological activity of fungus gardens
The Journal of Experimental Biology, 2014Co-Authors: Jon N. Seal, Morten Schiøtt, Ulrich G. MuellerAbstract:Fungus-gardening insects are among the most complex organisms because of their extensive co-evolutionary histories with obligate fungal symbionts and other microbes. Some fungus-gardening insect lineages share fungal symbionts with other members of their lineage and thus exhibit diffuse co-evolutionary relationships, while others exhibit little or no symbiont sharing, resulting in host–fungus fidelity. The mechanisms that maintain this symbiont fidelity are currently unknown. Prior work suggested that derived leaf-cutting ants in the genus Atta interact synergistically with leaf-cutter fungi ( Attamyces ) by exhibiting higher fungal growth rates and enzymatic activities than when growing a fungus from the sister-clade to Attamyces (so-called ‘Trachymyces’), grown primarily by the non-leaf cutting Trachymyrmex ants that form, correspondingly, the sister-clade to leaf-cutting ants. To elucidate the enzymatic bases of host–fungus specialization in leaf-cutting ants, we conducted a reciprocal fungus-switch experiment between the ant Atta texana and the ant Trachymyrmex arizonensis and report measured enzymatic activities of switched and sham-switched fungus gardens to digest starch, pectin, xylan, cellulose and casein. Gardens exhibited higher amylase and pectinase activities when A. texana ants cultivated Attamyces compared with Trachymyces fungi, consistent with enzymatic specialization. In contrast, gardens showed comparable amylase and pectinase activities when T. arizonensis cultivated either fungal species. Although gardens of leaf-cutting ants are not known to be significant metabolizers of cellulose, T. arizonensis were able to maintain gardens with significant cellulase activity when growing either fungal species. In contrast to carbohydrate metabolism, protease activity was significantly higher in Attamyces than in Trachymyces, regardless of the ant host. Activity of some enzymes employed by this symbiosis therefore arises from complex interactions between the ant host and the fungal symbiont.
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Co-evolution and the superorganism: switching cultivars does not alter the performance of fungus-gardening ant colonies
Functional Ecology, 2007Co-Authors: Jon N. Seal, Walter R. TschinkelAbstract:Summary 1 The fungus-gardening ants and their fungi represent a highly co-evolved, vertically transmitted mutualism. Mutualisms such as these are thought to be reciprocal antagonisms, so that the ants and the fungus can be expected to have some conflicting interests. 2 This paper reports the results from a cultivar switch experiment that documented the effects of switching the native cultivar from the basal ‘higher-attine’Trachymyrmex septentrionalis with a derived cultivar from the leaf-cutting ant, Atta texana. If the cultivars have been modified significantly during the adaptive radiation of this clade, then they should differ in their ability to produce ant and fungal biomass. If the ants can perceive differences in cultivar performance, then their food preference may also change as a result of the switch. Lastly, if conflict is present in this mutualism, then the sex ratio in the switched colonies should be male biased. 3 Our results showed that food preference was not altered by the new cultivar. The A. texana cultivar did not change the performance of T. septentrionalis colonies relative to colonies that were cultivating conspecific fungal cultivars. Foragers preferred insect faeces and oak staminate flowers over fresh leaves or flowers. Most variation in colony performance was attributable to substrate type. Sex ratio of offspring was not affected by fungal cultivar. With respect to fungal growth, the A. texana cultivar appeared to be more of a generalist, while the T. septentrionalis cultivar performed better on substrates preferred by the ants than those unpreferred. 4 The results of this study indicate that cooperation and not conflict has been more important in shaping the evolutionary ecology of this mutualism. Although the cultivars were certainly genetically and physiologically distinct, these differences did not account for variation in the production of ant biomass or ant behaviour. The emerging picture thus indicates that this mutualism should be viewed as a highly integrated superorganism that is more than the sum of its parts.
Heather D. Ishak - One of the best experts on this subject based on the ideXlab platform.
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Monoculture of Leafcutter Ant Gardens
2016Co-Authors: Ulrich G. Mueller, Heather D. Ishak, Jarrod J. Scott, Michael Cooper, Andre RodriguesAbstract:Background: Leafcutter 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 Findings: Using 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
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ecology of microfungal communities in gardens of fungus growing ants hymenoptera formicidae a year long survey of three species of attine ants in central texas
FEMS Microbiology Ecology, 2011Co-Authors: Ulrich G. Mueller, Andre Rodrigues, Maurício Bacci, Heather D. Ishak, Fernando C. PagnoccaAbstract:We profiled the microfungal communities in gardens of fungus-growing ants to evaluate possible species-specific ant-microfungal associations and to assess the potential dependencies of microfungal diversity on ant foraging behavior. In a 1-year survey, we isolated microfungi from nests of Cyphomyrmex wheeleri, Trachymyrmex septentrionalis and Atta texana in Central Texas. Microfungal prevalence was higher in gardens of C. wheeleri (57%) than in the gardens of T. septentrionalis (46%) and A. texana (35%). Culture-dependent methods coupled with a polyphasic approach of species identification revealed diverse and changing microfungal communities in all the sampling periods. Diversity analyses showed no obvious correlations between the number of observed microfungal species, ant species, or the ants' changing foraging behavior across the seasons. However, both correspondence analysis and 5.8S-rRNA gene unifrac analyses suggested structuring of microfungal communities by ant host. These host-specific differences may reflect in part the three different environments where ants were collected. Most interestingly, the specialized fungal parasite Escovopsis was not isolated from any attine garden in this study near the northernmost limit of the range of attine ants, contrasting with previous studies that indicated a significant incidence of this parasite in ant gardens from Central and South America. The observed differences of microfungal communities in attine gardens suggest that the ants are continuously in contact with a diverse microfungal species assemblage.
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Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant–fungus symbiosis
Proceedings of the National Academy of Sciences of the United States of America, 2011Co-Authors: Ulrich G. Mueller, Ruchira Sen, Heather D. Ishak, Alexander S. Mikheyev, Eunki Hong, Dan L. Warren, Scott E. Solomon, Mike Cooper, Jessica L. Miller, Kimberly A. ShafferAbstract:The obligate mutualism between leafcutter ants and their Attamyces fungi originated 8 to 12 million years ago in the tropics, but extends today also into temperate regions in South and North America. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the cold-sensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a south-to-north temperature gradient across the range of A. texana, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal, vertical garden relocation (maintaining gardens deep in the ground in winter to protect them from extreme cold, then moving gardens to warmer, shallow depths in spring). Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the original adaptations of this host-microbe symbiosis to tropical temperatures and the dependence on cold-sensitive fungal symbionts eventually constrained expansion into temperate habitats. Evolution of cold-tolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate host–microbe symbiosis.
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DOI:10.1111/j.1574-6941.2011.01152.x
2011Co-Authors: Andre Rodrigues, Ulrich G. Mueller, Heather D. Ishak, Maurı́cio Bacci, O C. Pagnocca, Correspondence Andre RodriguesAbstract:Escovopsis. We profiled the microfungal communities in gardens of fungus-growing ants to evaluate possible species-specific ant–microfungal associations and to assess the potential dependencies of microfungal diversity on ant foraging behavior. In a 1-year survey, we isolated microfungi from nests of Cyphomyrmex wheeleri, Trachymyrmex septentrionalis and Atta texana in Central Texas. Microfungal prevalence was higher in gardens of C. wheeleri (57%) than in the gardens of T. septentrionalis (46%) and A. texana (35%). Culture-dependent methods coupled with a polyphasic approach of species identification revealed diverse and changing microfungal communities in all the sampling periods. Diversity analyses showed no obvious correlations between the number of observed microfungal species, ant species, or the ants ’ changing foraging behavior across the seasons. However, both correspondence analysis and 5.8S-rRNA gene UNIFRAC analyses suggested structur-ing of microfungal communities by ant host. These host-specific differences ma
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Monoculture of Leafcutter Ant Gardens
PloS one, 2010Co-Authors: Ulrich G. Mueller, Heather D. Ishak, Jarrod J. Scott, Michael Cooper, Andre RodriguesAbstract:Background: Leafcutter 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 Findings: Using 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.
Andre Rodrigues - One of the best experts on this subject based on the ideXlab platform.
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Bacterial microbiomes from vertically transmitted fungal inocula of the leaf-cutting ant Atta texana.
Environmental Microbiology Reports, 2016Co-Authors: Lucas A. Meirelles, Quinn S. Mcfrederick, Andre Rodrigues, Joana D. Mantovani, Cynara De Melo Rodovalho, Henrique Ferreira, Maurício Bacci, Ulrich G. MuellerAbstract:Microbiome surveys provide clues for the functional roles of symbiotic microbial communities and their hosts. In this study, we elucidated bacterial microbiomes associated with the vertically transmitted fungal inocula (pellets) used by foundress queens of the leaf-cutting ant Atta texana as starter-cultures for new gardens. As reference microbiomes, we also surveyed bacterial microbiomes of foundress queens, gardens and brood of incipient nests. Pseudomonas, Acinetobacter, Propionibacterium and Corynebacterium were consistently present in high abundance in microbiomes. Some pellet and ant samples contained abundant bacteria from an Entomoplasmatales-clade, and a separate PCR-based survey of Entomoplasmatales bacteria in eight attine ant-genera from Brazil placed these bacteria in a monophyletic clade within the bacterial genus Mesoplasma. The attine ant-Mesoplasma association parallels a similar association between a closely related, monophyletic Entomoplasmatales-clade and army ants. Of thirteen A. texana nests surveyed, three nests with exceptionally high Mesoplasma abundance died, whereas the other nests survived. It is unclear whether Mesoplasma was the primary cause of mortality, or Mesoplasma became abundant in moribund nests for non-pathogenic reasons. However, the consistent and geographically widespread presence of Mesoplasma suggests an important functional role in the association with attine ants.
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Monoculture of Leafcutter Ant Gardens
2016Co-Authors: Ulrich G. Mueller, Heather D. Ishak, Jarrod J. Scott, Michael Cooper, Andre RodriguesAbstract:Background: Leafcutter 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 Findings: Using 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
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ecology of microfungal communities in gardens of fungus growing ants hymenoptera formicidae a year long survey of three species of attine ants in central texas
FEMS Microbiology Ecology, 2011Co-Authors: Ulrich G. Mueller, Andre Rodrigues, Maurício Bacci, Heather D. Ishak, Fernando C. PagnoccaAbstract:We profiled the microfungal communities in gardens of fungus-growing ants to evaluate possible species-specific ant-microfungal associations and to assess the potential dependencies of microfungal diversity on ant foraging behavior. In a 1-year survey, we isolated microfungi from nests of Cyphomyrmex wheeleri, Trachymyrmex septentrionalis and Atta texana in Central Texas. Microfungal prevalence was higher in gardens of C. wheeleri (57%) than in the gardens of T. septentrionalis (46%) and A. texana (35%). Culture-dependent methods coupled with a polyphasic approach of species identification revealed diverse and changing microfungal communities in all the sampling periods. Diversity analyses showed no obvious correlations between the number of observed microfungal species, ant species, or the ants' changing foraging behavior across the seasons. However, both correspondence analysis and 5.8S-rRNA gene unifrac analyses suggested structuring of microfungal communities by ant host. These host-specific differences may reflect in part the three different environments where ants were collected. Most interestingly, the specialized fungal parasite Escovopsis was not isolated from any attine garden in this study near the northernmost limit of the range of attine ants, contrasting with previous studies that indicated a significant incidence of this parasite in ant gardens from Central and South America. The observed differences of microfungal communities in attine gardens suggest that the ants are continuously in contact with a diverse microfungal species assemblage.
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DOI:10.1111/j.1574-6941.2011.01152.x
2011Co-Authors: Andre Rodrigues, Ulrich G. Mueller, Heather D. Ishak, Maurı́cio Bacci, O C. Pagnocca, Correspondence Andre RodriguesAbstract:Escovopsis. We profiled the microfungal communities in gardens of fungus-growing ants to evaluate possible species-specific ant–microfungal associations and to assess the potential dependencies of microfungal diversity on ant foraging behavior. In a 1-year survey, we isolated microfungi from nests of Cyphomyrmex wheeleri, Trachymyrmex septentrionalis and Atta texana in Central Texas. Microfungal prevalence was higher in gardens of C. wheeleri (57%) than in the gardens of T. septentrionalis (46%) and A. texana (35%). Culture-dependent methods coupled with a polyphasic approach of species identification revealed diverse and changing microfungal communities in all the sampling periods. Diversity analyses showed no obvious correlations between the number of observed microfungal species, ant species, or the ants ’ changing foraging behavior across the seasons. However, both correspondence analysis and 5.8S-rRNA gene UNIFRAC analyses suggested structur-ing of microfungal communities by ant host. These host-specific differences ma
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Monoculture of Leafcutter Ant Gardens
PloS one, 2010Co-Authors: Ulrich G. Mueller, Heather D. Ishak, Jarrod J. Scott, Michael Cooper, Andre RodriguesAbstract:Background: Leafcutter 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 Findings: Using 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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Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant–fungus symbiosis
Proceedings of the National Academy of Sciences of the United States of America, 2011Co-Authors: Ulrich G. Mueller, Ruchira Sen, Heather D. Ishak, Alexander S. Mikheyev, Eunki Hong, Dan L. Warren, Scott E. Solomon, Mike Cooper, Jessica L. Miller, Kimberly A. ShafferAbstract:The obligate mutualism between leafcutter ants and their Attamyces fungi originated 8 to 12 million years ago in the tropics, but extends today also into temperate regions in South and North America. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the cold-sensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a south-to-north temperature gradient across the range of A. texana, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal, vertical garden relocation (maintaining gardens deep in the ground in winter to protect them from extreme cold, then moving gardens to warmer, shallow depths in spring). Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the original adaptations of this host-microbe symbiosis to tropical temperatures and the dependence on cold-sensitive fungal symbionts eventually constrained expansion into temperate habitats. Evolution of cold-tolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate host–microbe symbiosis.
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Construction of chimaeric gardens through fungal intercropping: a symbiont choice experiment in the leafcutter ant Atta texana (Attini, Formicidae)
Behavioral Ecology and Sociobiology, 2010Co-Authors: Ruchira Sen, Heather D. Ishak, Trevor R. Kniffin, Ulrich G. MuellerAbstract:Interspecies or intraspecies cooperation can be stabilized evolutionarily if choosing partners favor beneficial partners and discriminate against non-beneficial partners. We quantified such partner choice (symbiont choice) in the leafcutter ant Atta texana (Attini, Formicidae) by presenting the ants in a cafeteria-style preference assay with genotypically distinct fungal cultivars from A. texana and Acromyrmex versicolor . Symbiont choice was measured as the ants' tendency to choose one or more cultivar(s) from several pure (axenic) cultivar fragments and convert a given fungal fragment into a garden. Microsatellite DNA fingerprinting enabled us to identify the cultivars chosen by the ants for their gardens. In 91% of the choice tests, A. texana workers combined multiple cultivars into a single intercropped, chimaeric garden, and the cultivars coexisted in such chimaeric gardens for as long as 4 months. Coexistence of distinct fungal genotypes in chimaeric gardens appears to contradict a recent model of cultivar competition postulating that each cultivar secretes incompatibility compounds harming other cultivars, which presumably would preclude the intercropped polyculture observed in our experiments. Although we found no clear evidence of novel, recombinant genotypes in the experimental chimaeric gardens, the intercropping of cultivar genotypes may occasionally lead under natural conditions to exchange of genetic material between coexisting cultivars, thus introducing novel cultivar genotypes into the leafcutter symbiosis. Symbiont choice by ants and any competition between coexisting cultivar strains in chimaeric gardens do not appear to operate fast enough in our laboratory assay to convert chimaeric gardens into the monocultures observed for A . texana under natural conditions.