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Jacobus J. Boomsma - One of the best experts on this subject based on the ideXlab platform.
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differential immune gene expression in sperm storage organs of leaf cutting Ants
The Journal of Experimental Biology, 2018Co-Authors: Morten Schiøtt, Sarah Cherasse, Boris Baer, Jacobus J. BoomsmaAbstract:Leaf-Cutting ant queens mate with multiple males during a single nuptial flight and store sperm for up to two decades. During mating, males transfer sperm from their accessory testes to the queen bursa copulatrix from where it enters the spermatheca, an insect sperm storage organ that has become highly specialized in long-lived ant queens who never re-mate later in life. Long-term storage without the possibility to obtain new sperm creates an immune defence dilemma, because recognition of non-self cells eliminates infections but may also target irreplaceable sperm and reduce lifetime reproductive success. We therefore hypothesized that non-specific immune responses, like pathogen melanization, should be silenced in the spermatheca, because they rely on general non-self recognition, and that specific responses such as antimicrobial peptides are activated instead as they specifically target pathogenic bacteria and/or fungi. The maintenance of uninfected sperm cells by males before mating is not constrained by non-self recognition, meaning immune regulation might be more liberal in male reproductive organs. To test this hypothesis, we measured gene expression of two antimicrobial peptides, abaecin and defensin, and prophenoloxidase, an important enzyme of the melanization pathway, in male accessory glands and testes and in queen bursae copulatrix and spermathecae of Acromyrmex echinatior and Atta colombica Leaf-Cutting Ants. As expected, prophenoloxidase expression was low in reproductive organs that sustain prolonged contact with sperm, whereas antimicrobial peptides showed average to high expression, indicating that Leaf-Cutting Ants invest in specific rather than generalist immune defences for pathogen protection in organs that store sperm.
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Differences in Forage-Acquisition and Fungal Enzyme Activity Contribute to Niche Segregation in Panamanian Leaf-Cutting Ants
2016Co-Authors: Pepijn W. Kooij, Morten Schiøtt, Joanito Liberti, Konstantinos Giampoudakis, Jacobus J. BoomsmaAbstract:The genera Atta and Acromyrmex are often grouped as Leaf-Cutting Ants for pest management assessments and ecological surveys, although their mature colony sizes and foraging niches may differ substantially. Few studies have addressed such interspecific differences at the same site, which prompted us to conduct a comparative study across six sympatric Leaf-Cutting ant species in Central Panama. We show that foraging rates during the transition between dry and wet season differ about 60 fold between genera, but are relatively constant across species within genera. These differences appear to match overall differences in colony size, especially when Atta workers that return to their nests without leaves are assumed to carry liquid food. We confirm that Panamanian Atta specialize primarily on tree-leaves whereas Acromyrmex focus on collecting flowers and herbal leaves and that species within genera are similar in these overall foraging strategies. Species within genera tended to be spaced out over the three habitat categories that we distinguished (forest, forest edge, open grassland), but each of these habitats normally had only a single predominant Atta and Acromyrmex species. We measured activities of twelve fungus garden decomposition enzymes, belonging to the amylases, cellulases, hemicellulases, pectinases and proteinases, and show that average enzyme activity per unit of fungal mass in Atta gardens is lower than in Acromyrmex gardens. Expression profiles of fungal enzymes in Atta also appeared to be more specialized than in Acromyrmex, possibly reflecting variation in forage material. Our results suggest that species- and genus-level identities of Leaf-Cutting Ants an
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Acromyrmex Leaf-Cutting Ants Have Simple Gut Microbiota with Nitrogen-Fixing Potential
Applied and Environmental Microbiology, 2015Co-Authors: Panagiotis Sapountzis, Mariya Zhukova, Lars Hestbjerg Hansen, Søren J. Sørensen, Morten Schiøtt, Jacobus J. BoomsmaAbstract:Ants and termites have independently evolved obligate fungus-farming mutualisms, but their gardening procedures are fundamentally different, as the termites predigest their plant substrate whereas the Ants deposit it directly on the fungus garden. Fungus-growing termites retained diverse gut microbiota, but bacterial gut communities in fungus-growing Leaf-Cutting Ants have not been investigated, so it is unknown whether and how they are specialized on an exclusively fungal diet. Here we characterized the gut bacterial community of Panamanian Acromyrmex species, which are dominated by only four bacterial taxa: Wolbachia, Rhizobiales, and two Entomoplasmatales taxa. We show that the Entomoplasmatales can be both intracellular and extracellular across different gut tissues, Wolbachia is mainly but not exclusively intracellular, and the Rhizobiales species is strictly extracellular and confined to the gut lumen, where it forms biofilms along the hindgut cuticle supported by an adhesive matrix of polysaccharides. Tetracycline diets eliminated the Entomoplasmatales symbionts but hardly affected Wolbachia and only moderately reduced the Rhizobiales, suggesting that the latter are protected by the biofilm matrix. We show that the Rhizobiales symbiont produces bacterial NifH proteins that have been associated with the fixation of nitrogen, suggesting that these compartmentalized hindgut symbionts alleviate nutritional constraints emanating from an exclusive fungus garden diet reared on a substrate of leaves.
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Somatic incompatibility and genetic structure of fungal crops in sympatric Atta colombica and Acromyrmex echinatior Leaf-Cutting Ants.
Fungal ecology, 2015Co-Authors: Pepijn W. Kooij, Morten Schiøtt, Michael Poulsen, Jacobus J. BoomsmaAbstract:Obligate mutualistic symbioses rely on mechanisms that secure host-symbiont commitments to maximize host benefits and prevent symbiont cheating. Previous studies showed that somatic incompatibilities correlate with neutral-marker-based genetic distances between fungal symbionts of Panamanian Acromyrmex Leaf-Cutting Ants, but the extent to which this relationship applies more generally remained unclear. Here we showed that genetic distances accurately predicted somatic incompatibility for Acromyrmex echinatior symbionts irrespective of whether neutral microsatellites or AFLP markers were used, but that such correlations were weaker or absent in sympatric Atta colombica colonies. Further analysis showed that the symbiont clades maintained by A. echinatior and A. colombica were likely to represent separate gene pools, so that neutral markers were unlikely to be similarly correlated with incompatibility loci that have experienced different selection regimes. We suggest that evolutionarily derived claustral colony founding by Atta queens may have removed selection for strong incompatibility in Atta fungi, as this condition makes the likelihood of symbiont swaps much lower than in Acromyrmex, where incipient nests stay open because queens have to forage until the first workers emerge.
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The fungal symbiont of Acromyrmex Leaf-Cutting Ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides
BMC genomics, 2013Co-Authors: Morten Nedergaard Grell, Jacobus J. Boomsma, Tore Linde, Sanne Nygaard, Kåre Lehmann Nielsen, Lene LangeAbstract:The fungus gardens of Leaf-Cutting Ants are natural biomass conversion systems that turn fresh plant forage into fungal biomass to feed the farming Ants. However, the decomposition potential of the symbiont Leucocoprinus gongylophorus for processing polysaccharides has remained controversial. We therefore used quantifiable DeepSAGE technology to obtain mRNA expression patterns of genes coding for secreted enzymes from top, middle, and bottom sections of a laboratory fungus-garden of Acromyrmex echinatior Leaf-Cutting Ants. A broad spectrum of biomass-conversion-relevant enzyme genes was found to be expressed in situ: cellulases (GH3, GH5, GH6, GH7, AA9 [formerly GH61]), hemicellulases (GH5, GH10, CE1, GH12, GH74), pectinolytic enzymes (CE8, GH28, GH43, PL1, PL3, PL4), glucoamylase (GH15), α-galactosidase (GH27), and various cutinases, esterases, and lipases. In general, expression of these genes reached maximal values in the bottom section of the garden, particularly for an AA9 lytic polysaccharide monooxygenase and for a GH5 (endocellulase), a GH7 (reducing end-acting cellobiohydrolase), and a GH10 (xylanase), all containing a carbohydrate binding module that specifically binds cellulose (CBM1). Although we did not directly quantify enzyme abundance, the profile of expressed cellulase genes indicates that both hydrolytic and oxidative degradation is taking place. The fungal symbiont of Acromyrmex Leaf-Cutting Ants can degrade a large range of plant polymers, but the conversion of cellulose, hemicellulose, and part of the pectin occurs primarily towards the end of the decomposition process, i.e. in the bottom section of the fungus garden. These conversions are likely to provide nutrients for the fungus itself rather than for the Ants, whose colony growth and reproductive success are limited by proteins obtained from ingesting fungal gongylidia. These specialized hyphal tips are hardly produced in the bottom section of fungus gardens, consistent with the Ants discarding old fungal biomass from this part of the garden. The transcripts that we found suggest that actively growing mycelium in the bottom of gardens helps to maintain an optimal water balance to avoid hyphal disintegration, so the Ants can ultimately discard healthy rather than decaying and diseased garden material, and to buffer negative effects of varying availability and quality of substrate across the seasons.
Flavio Roces - One of the best experts on this subject based on the ideXlab platform.
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appetitive and aversive learning of plAnts odors inside different nest compartments by foraging leaf cutting Ants
Journal of Insect Physiology, 2018Co-Authors: Andres Arenas, Flavio RocesAbstract:Cues inside the nest provide social insect foragers with information about resources currently exploited that may influence their decisions outside. Leaf-Cutting Ants harvest leaf fragments that are either further processed as substrate for their symbiotic fungus, or disposed of if unsuitable. We investigated whether Acromyrmex ambiguus foragers develop learned preferences for olfactory cues they experienced either in the fungus or in the waste chamber of the nest. Foragers' olfactory preferences were quantified as a choice between sugared papers disks scented with a novel odor and with the odor experienced in one of the nest compartments, before and after odor addition. Odors incorporated in the fungus chamber led to preferences towards paper disks smelling of them. Conversely, odors experienced in the waste chambers led to avoidance of similarly-scented disks. To investigate context-specificity of responses, we quantified learned preferences towards an odor that occurred first in the fungus chamber, and 14 h later in the waste chamber. Foragers initially developed a preference for the odor added in the fungus chamber that turned into avoidance when the same odor solely occurred later in the waste chamber. Avoidance of plAnts could also be induced in a more natural context, when fresh leaf disks of novel plAnts, privet or firethorn, were presented in the waste chamber. We conclude that learned acceptance or rejection of suitable plAnts by foragers depend on the learning context: smells can lead to appetitive learning when present in the fungus garden, or to avoidance learning when they occur at the dump.
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the construction of ventilation turrets in atta vollenweideri leaf cutting Ants carbon dioxide levels in the nest tunnels but not airflow or air humidity influence turret structure
PLOS ONE, 2017Co-Authors: Florian Halboth, Flavio RocesAbstract:Nest ventilation in the Leaf-Cutting ant Atta vollenweideri is driven via a wind-induced mechanism. On their nests, workers construct small turrets that are expected to facilitate nest ventilation. We hypothesized that the construction and structural features of the turrets would depend on the colony’s current demands for ventilation and thus might be influenced by the prevailing environmental conditions inside the nest. Therefore, we tested whether climate-related parameters, namely airflow, air humidity and CO2 levels in the outflowing nest air influenced turret construction in Atta vollenweideri. In the laboratory, we simulated a semi-natural nest arrangement with fungus chambers, a central ventilation tunnel providing outflow of air and an aboveground building arena for turret construction. In independent series, different climatic conditions inside the ventilation tunnel were experimentally generated, and after 24 hours, several features of the built turret were quantified, i.e., mass, height, number and surface area (aperture) of turret openings. Turret mass and height were similar in all experiments even when no airflow was provided in the ventilation tunnel. However, elevated CO2 levels led to the construction of a turret with several minor openings and a larger total aperture. This effect was statistically significant at higher CO2 levels of 5% and 10% but not at 1% CO2. The construction of a turret with several minor openings did not depend on the strong differences in CO2 levels between the outflowing and the outside air, since workers also built permeated turrets even when the CO2 levels inside and outside were both similarly high. We propose that the construction of turrets with several openings and larger opening surface area might facilitate the removal of CO2 from the underground nest structure and could therefore be involved in the control of nest climate in Leaf-Cutting Ants.
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underground anemotactic orientation in leaf cutting Ants perception of airflow and experience dependent choice of airflow direction during digging
Naturwissenschaften, 2017Co-Authors: Florian Halboth, Flavio RocesAbstract:Air exchange between the large nests of Atta vollenweideri Leaf-Cutting Ants and the environment strongly relies on a passive, wind-induced ventilation mechanism. Air moves through nest tunnels and airflow direction depends on the location of the tunnel openings on the nest mound. We hypothesized that Ants might use the direction of airflow along nest tunnels as orientation cue in the context of climate control, as digging workers might prefer to broaden or to close tunnels with inflowing or outflowing air in order to regulate nest ventilation. To investigate anemotactic orientation in Atta vollenweideri, we first tested the Ants’ ability to perceive air movements by confronting single workers with airflow stimuli in the range 0 to 20 cm/s. Workers responded to airflow velocities ≥ 2 cm/s, and the number of Ants reacting to the stimulus increased with increasing airflow speed. Second, we asked whether digging workers use airflow direction as an orientation cue. Workers were exposed to either inflow or outflow of air while digging in the nest and could subsequently choose between two digging sites providing either inflow or outflow of air, respectively. Workers significantly chose the side with the same airflow direction they experienced before. When no airflow was present during initial digging, workers showed no preference for airflow directions. Workers developed preferences for airflow direction only after previous exposure to a given airflow direction. We suggest that experience-modified anemotaxis might help Leaf-Cutting Ants spatially organize their digging activity inside the nest during tasks related to climate control.
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avoidance of plAnts unsuitable for the symbiotic fungus in leaf cutting Ants learning can take place entirely at the colony dump
PLOS ONE, 2017Co-Authors: Andres Arenas, Flavio RocesAbstract:PlAnts initially accepted by foraging Leaf-Cutting Ants are later avoided if they prove unsuitable for their symbiotic fungus. Plant avoidance is mediated by the waste produced in the fungus garden soon after the incorporation of the unsuitable leaves, as foragers can learn plant odors and cues from the damaged fungus that are both present in the recently produced waste particles. We asked whether avoidance learning of plAnts unsuitable for the symbiotic fungus can take place entirely at the colony dump. In order to investigate whether cues available in the waste chamber induce plant avoidance in naive subcolonies, we exchanged the waste produced by subcolonies fed either fungicide-treated privet leaves or untreated leaves and measured the acceptance of untreated privet leaves before and after the exchange of waste. Second, we evaluated whether foragers could perceive the avoidance cues directly at the dump by quantifying the visits of labeled foragers to the waste chamber. Finally, we asked whether foragers learn to specifically avoid untreated leaves of a plant after a confinement over 3 hours in the dump of subcolonies that were previously fed fungicide-treated leaves of that species. After the exchange of the waste chambers, workers from subcolonies that had access to waste from fungicide-treated privet leaves learned to avoid that plant. One-third of the labeled foragers visited the dump. Furthermore, naive foragers learned to avoid a specific, previously unsuitable plant if exposed solely to cues of the dump during confinement. We suggest that cues at the dump enable foragers to predict the unsuitable effects of plAnts even if they had never been experienced in the fungus garden.
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Carbon dioxide sensing in an obligate insect-fungus symbiosis: CO2 preferences of Leaf-Cutting Ants to rear their mutualistic fungus
2017Co-Authors: Daniela Römer, Martin Bollazzi, Flavio RocesAbstract:Defense against biotic or abiotic stresses is one of the benefits of living in symbiosis. Leaf-Cutting Ants, which live in an obligate mutualism with a fungus, attenuate thermal and desiccation stress of their partner through behavioral responses, by choosing suitable places for fungus-rearing across the soil profile. The underground environment also presents hypoxic (low oxygen) and hypercapnic (high carbon dioxide) conditions, which can negatively influence the symbiont. Here, we investigated whether workers of the Leaf-Cutting ant Acromyrmex lundii use the CO2 concentration as an orientation cue when selecting a place to locate their fungus garden, and whether they show preferences for specific CO2 concentrations. We also evaluated whether levels preferred by workers for fungus-rearing differ from those selected for themselves. In the laboratory, CO2 preferences were assessed in binary choices between chambers with different CO2 concentrations, by quantifying number of workers in each chamber and amount of relocated fungus. Leaf-Cutting Ants used the CO2 concentration as a spatial cue when selecting places for fungus-rearing. A. lundii preferred intermediate CO2 levels, between 1 and 3%, as they would encounter at soil depths where their nest chambers are located. In addition, workers avoided both atmospheric and high CO2 levels as they would occur outside the nest and at deeper soil layers, respectively. In order to prevent fungus desiccation, however, workers relocated fungus to high CO2 levels, which were otherwise avoided. Workers’ CO2 preferences for themselves showed no clear-cut pattern. We suggest that workers avoid both atmospheric and high CO2 concentrations not because they are detrimental for themselves, but because of their consequences for the symbiotic partner. Whether the preferred CO2 concentrations are beneficial for symbiont growth remains to be investigated, as well as whether the observed preferences for fungus-rearing influences the Ants’ decisions where to excavate new chambers across the soil profile.
Morten Schiøtt - One of the best experts on this subject based on the ideXlab platform.
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differential immune gene expression in sperm storage organs of leaf cutting Ants
The Journal of Experimental Biology, 2018Co-Authors: Morten Schiøtt, Sarah Cherasse, Boris Baer, Jacobus J. BoomsmaAbstract:Leaf-Cutting ant queens mate with multiple males during a single nuptial flight and store sperm for up to two decades. During mating, males transfer sperm from their accessory testes to the queen bursa copulatrix from where it enters the spermatheca, an insect sperm storage organ that has become highly specialized in long-lived ant queens who never re-mate later in life. Long-term storage without the possibility to obtain new sperm creates an immune defence dilemma, because recognition of non-self cells eliminates infections but may also target irreplaceable sperm and reduce lifetime reproductive success. We therefore hypothesized that non-specific immune responses, like pathogen melanization, should be silenced in the spermatheca, because they rely on general non-self recognition, and that specific responses such as antimicrobial peptides are activated instead as they specifically target pathogenic bacteria and/or fungi. The maintenance of uninfected sperm cells by males before mating is not constrained by non-self recognition, meaning immune regulation might be more liberal in male reproductive organs. To test this hypothesis, we measured gene expression of two antimicrobial peptides, abaecin and defensin, and prophenoloxidase, an important enzyme of the melanization pathway, in male accessory glands and testes and in queen bursae copulatrix and spermathecae of Acromyrmex echinatior and Atta colombica Leaf-Cutting Ants. As expected, prophenoloxidase expression was low in reproductive organs that sustain prolonged contact with sperm, whereas antimicrobial peptides showed average to high expression, indicating that Leaf-Cutting Ants invest in specific rather than generalist immune defences for pathogen protection in organs that store sperm.
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Differences in Forage-Acquisition and Fungal Enzyme Activity Contribute to Niche Segregation in Panamanian Leaf-Cutting Ants
2016Co-Authors: Pepijn W. Kooij, Morten Schiøtt, Joanito Liberti, Konstantinos Giampoudakis, Jacobus J. BoomsmaAbstract:The genera Atta and Acromyrmex are often grouped as Leaf-Cutting Ants for pest management assessments and ecological surveys, although their mature colony sizes and foraging niches may differ substantially. Few studies have addressed such interspecific differences at the same site, which prompted us to conduct a comparative study across six sympatric Leaf-Cutting ant species in Central Panama. We show that foraging rates during the transition between dry and wet season differ about 60 fold between genera, but are relatively constant across species within genera. These differences appear to match overall differences in colony size, especially when Atta workers that return to their nests without leaves are assumed to carry liquid food. We confirm that Panamanian Atta specialize primarily on tree-leaves whereas Acromyrmex focus on collecting flowers and herbal leaves and that species within genera are similar in these overall foraging strategies. Species within genera tended to be spaced out over the three habitat categories that we distinguished (forest, forest edge, open grassland), but each of these habitats normally had only a single predominant Atta and Acromyrmex species. We measured activities of twelve fungus garden decomposition enzymes, belonging to the amylases, cellulases, hemicellulases, pectinases and proteinases, and show that average enzyme activity per unit of fungal mass in Atta gardens is lower than in Acromyrmex gardens. Expression profiles of fungal enzymes in Atta also appeared to be more specialized than in Acromyrmex, possibly reflecting variation in forage material. Our results suggest that species- and genus-level identities of Leaf-Cutting Ants an
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Acromyrmex Leaf-Cutting Ants Have Simple Gut Microbiota with Nitrogen-Fixing Potential
Applied and Environmental Microbiology, 2015Co-Authors: Panagiotis Sapountzis, Mariya Zhukova, Lars Hestbjerg Hansen, Søren J. Sørensen, Morten Schiøtt, Jacobus J. BoomsmaAbstract:Ants and termites have independently evolved obligate fungus-farming mutualisms, but their gardening procedures are fundamentally different, as the termites predigest their plant substrate whereas the Ants deposit it directly on the fungus garden. Fungus-growing termites retained diverse gut microbiota, but bacterial gut communities in fungus-growing Leaf-Cutting Ants have not been investigated, so it is unknown whether and how they are specialized on an exclusively fungal diet. Here we characterized the gut bacterial community of Panamanian Acromyrmex species, which are dominated by only four bacterial taxa: Wolbachia, Rhizobiales, and two Entomoplasmatales taxa. We show that the Entomoplasmatales can be both intracellular and extracellular across different gut tissues, Wolbachia is mainly but not exclusively intracellular, and the Rhizobiales species is strictly extracellular and confined to the gut lumen, where it forms biofilms along the hindgut cuticle supported by an adhesive matrix of polysaccharides. Tetracycline diets eliminated the Entomoplasmatales symbionts but hardly affected Wolbachia and only moderately reduced the Rhizobiales, suggesting that the latter are protected by the biofilm matrix. We show that the Rhizobiales symbiont produces bacterial NifH proteins that have been associated with the fixation of nitrogen, suggesting that these compartmentalized hindgut symbionts alleviate nutritional constraints emanating from an exclusive fungus garden diet reared on a substrate of leaves.
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Somatic incompatibility and genetic structure of fungal crops in sympatric Atta colombica and Acromyrmex echinatior Leaf-Cutting Ants.
Fungal ecology, 2015Co-Authors: Pepijn W. Kooij, Morten Schiøtt, Michael Poulsen, Jacobus J. BoomsmaAbstract:Obligate mutualistic symbioses rely on mechanisms that secure host-symbiont commitments to maximize host benefits and prevent symbiont cheating. Previous studies showed that somatic incompatibilities correlate with neutral-marker-based genetic distances between fungal symbionts of Panamanian Acromyrmex Leaf-Cutting Ants, but the extent to which this relationship applies more generally remained unclear. Here we showed that genetic distances accurately predicted somatic incompatibility for Acromyrmex echinatior symbionts irrespective of whether neutral microsatellites or AFLP markers were used, but that such correlations were weaker or absent in sympatric Atta colombica colonies. Further analysis showed that the symbiont clades maintained by A. echinatior and A. colombica were likely to represent separate gene pools, so that neutral markers were unlikely to be similarly correlated with incompatibility loci that have experienced different selection regimes. We suggest that evolutionarily derived claustral colony founding by Atta queens may have removed selection for strong incompatibility in Atta fungi, as this condition makes the likelihood of symbiont swaps much lower than in Acromyrmex, where incipient nests stay open because queens have to forage until the first workers emerge.
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differential gene expression in acromyrmex leaf cutting Ants after challenges with two fungal pathogens
Molecular Ecology, 2013Co-Authors: Sze Huei Yek, Jacobus J. Boomsma, Morten SchiøttAbstract:Social insects in general and Leaf-Cutting Ants in particular have increased selection pressures on their innate immune system due to their social lifestyle and monoclonality of the symbiotic fungal cultivar. As this symbiosis is obligate for both parties, prophylactic behavioural defences against infections are expected to increase either ant survival or fungus-garden survival, but also to possibly trade off when specific infections differ in potential danger. We examined the effectiveness of prophylactic behaviours and modulations of innate immune defences by a combination of inoculation bioassays and genome-wide transcriptomic studies (RNA-Seq), using an ant pathogen (Metarhizium brunneum) and a fungus-garden pathogen (Escovopsis weberi) and administering inoculations both directly and indirectly (via the symbiotic partner). Upon detection of pathogen conidia, ant workers responded by increasing both general activity and the frequency of specific defence behaviours (self-grooming, allo-grooming, garden-grooming) independent of the pathogen encountered. This trend was also evident in the patterns of gene expression change. Both direct and indirect (via fungus garden) inoculations with Metarhizium induced a general up-regulation of gene expression, including a number of well-known immune-related genes. In contrast, direct inoculation of the fungus garden by Escovopsis induced an overall down-regulation of ant gene expression, whereas indirect inoculation (via the Ants) did not, suggesting that increased activity of Ants to remove this fungus-garden pathogen is costly and involves trade-offs with the activation of other physiological pathways.
Michael Poulsen - One of the best experts on this subject based on the ideXlab platform.
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Preliminary in vitro insights into the use of natural fungal pathogens of Leaf-Cutting Ants as biocontrol agents
2020Co-Authors: Patricia Folgarait, Michael Poulsen, Norma Gorosito, Cameron R. CurrieAbstract:Abstract Leaf-Cutting Ants are one of the mai
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Somatic incompatibility and genetic structure of fungal crops in sympatric Atta colombica and Acromyrmex echinatior Leaf-Cutting Ants.
Fungal ecology, 2015Co-Authors: Pepijn W. Kooij, Morten Schiøtt, Michael Poulsen, Jacobus J. BoomsmaAbstract:Obligate mutualistic symbioses rely on mechanisms that secure host-symbiont commitments to maximize host benefits and prevent symbiont cheating. Previous studies showed that somatic incompatibilities correlate with neutral-marker-based genetic distances between fungal symbionts of Panamanian Acromyrmex Leaf-Cutting Ants, but the extent to which this relationship applies more generally remained unclear. Here we showed that genetic distances accurately predicted somatic incompatibility for Acromyrmex echinatior symbionts irrespective of whether neutral microsatellites or AFLP markers were used, but that such correlations were weaker or absent in sympatric Atta colombica colonies. Further analysis showed that the symbiont clades maintained by A. echinatior and A. colombica were likely to represent separate gene pools, so that neutral markers were unlikely to be similarly correlated with incompatibility loci that have experienced different selection regimes. We suggest that evolutionarily derived claustral colony founding by Atta queens may have removed selection for strong incompatibility in Atta fungi, as this condition makes the likelihood of symbiont swaps much lower than in Acromyrmex, where incipient nests stay open because queens have to forage until the first workers emerge.
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interaction between workers during a short time window is required for bacterial symbiont transmission in acromyrmex leaf cutting Ants
PLOS ONE, 2014Co-Authors: Sarah E Marsh, Michael Poulsen, Cameron R. Currie, Adrian A PintotomasAbstract:Stable associations between partners over time are critical for the evolution of mutualism. Hosts employ a variety of mechanisms to maintain specificity with bacterial associates. Acromyrmex Leaf-Cutting Ants farm a fungal cultivar as their primary nutrient source. These Ants also carry a Pseudonocardia Actinobacteria exosymbiont on their bodies that produces antifungal compounds that help inhibit specialized parasites of the Ants' fungal garden. Major workers emerge from their pupal cases (eclose) symbiont-free, but exhibit visible Actinobacterial coverage within 14 days post-eclosion. Using subcolony experiments, we investigate exosymbiont transmission within Acromyrmex colonies. We found successful transmission to newly eclosed major workers fostered by major workers with visible Actinobacteria in all cases (100% acquiring, n=19). In contrast, newly eclosed major workers reared without exosymbiont-carrying major workers did not acquire visible Actinobacteria (0% acquiring, n=73). We further show that the majority of Ants exposed to major workers with exosymbionts within 2 hours of eclosion acquired bacteria (60.7% acquiring, n=28), while normal acquisition did not occur when exposure occurred later than 2 hours post-eclosion (0% acquiring, n=18). Our findings show that transmission of exosymbionts to newly eclosed major workers occurs through interactions with exosymbiont-covered workers within a narrow time window after eclosion. This mode of transmission likely helps ensure the defensive function within colonies, as well as specificity and partner fidelity in the ant-bacterium association.
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caste specialization in behavioral defenses against fungus garden parasites in acromyrmex octospinosus leaf cutting Ants
Insectes Sociaux, 2011Co-Authors: D Abramowski, Cameron R. Currie, Michael PoulsenAbstract:Division of labor and caste specialization plays an important role in many aspects of social insect colony organization, including parasite defense. Within Leaf-Cutting ant colonies, worker caste specialization permeates colony tasks ranging from foraging, substrate incorporation, brood care, and chemical defenses via glandular secretions and mutualistic bacteria. Leaf-Cutting Ants rely on protecting a mutualistic fungus they grow for food from microfungi in the genus Escovopsis that parasitizes the ant–fungus relationship. Here, we examine whether Acromyrmex octospinosus leaf-cutter ant castes (minors and majors) display task specialization in two behavioral defenses against Escovopsis: fungus grooming (the removal of Escovopsis spores) and weeding (the removal of large pieces of Escovopsis-infected fungus garden). Using behavioral observations, we show that minors are the primary caste that performs fungus grooming, while weeding is almost exclusively performed by majors. In addition, using a sub-colony infection experimental setup, we show that at the early stages of infection, minors more efficiently remove Escovopsis spores from the fungus garden, thereby restricting Escovopsis spore germination and growth. At later stages of infection, after Escovopsis spore germination, we find that major workers are as efficient as minors in defending the fungus garden, likely due to the increased importance of weeding. Finally, we show, using SEM imaging, that the number of sensory structures is similar between minor and major workers. If these structures are invoked in recognition of the parasites, this finding suggests that both castes are able to sense Escovopsis. Our findings support that leaf-cutter ant behavioral defense tasks against Escovopsis are subject to caste specialization, likely facilitated by worker sizes being optimal for grooming and weeding by minors and majors, respectively, with important consequences for cultivar defense.
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The role of symbiont genetic distance and potential adaptability in host preference towards Pseudonocardia symbionts in Acromyrmex Leaf-Cutting Ants.
Journal of insect science (Online), 2011Co-Authors: Michael Poulsen, Janielle Maynard, Damien L Roland, Cameron R. CurrieAbstract:Fungus-growing Ants display symbiont preference in behavioral assays, both towards the fungus they cultivate for food and Actinobacteria they maintain on their cuticle for antibiotic production against parasites. These Actinobacteria, genus Pseudonocardia Henssen (Pseudonocardiacea: Actinomycetales), help defend the Ants' fungal mutualist from specialized parasites. In Acromyrmex Mayr (Hymenoptera: Formicidae) Leaf-Cutting Ants, individual colonies maintain either a single or a few strains of Pseudonocardia, and the symbiont is primarily vertically transmitted between generations by colony-founding queens. A recent report found that Acromyrmex workers are able to differentiate between their native Pseudonocardia strain and non-native strains isolated from sympatric or allopatric Acromyrmex species, and show preference for their native strain. Here we explore worker preference when presented with two non-native strains, elucidating the role of genetic distance on preference between strains and Pseudonocardia origin. Our findings suggest that Ants tend to prefer bacteria more closely related to their native bacterium and that genetic similarity is probably more important than whether symbionts are ant-associated or free-living. Preliminary findings suggest that when continued exposure to a novel Pseudonocardia strain occurs, ant symbiont preference is potentially adaptable, with colonies apparently being able to alter symbiont preference over time. These findings are discussed in relation to the role of adaptive recognition, potential ecological flexibility in symbiont preference, and more broadly, in relation to self versus non-self recognition.
Cameron R. Currie - One of the best experts on this subject based on the ideXlab platform.
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Preliminary in vitro insights into the use of natural fungal pathogens of Leaf-Cutting Ants as biocontrol agents
2020Co-Authors: Patricia Folgarait, Michael Poulsen, Norma Gorosito, Cameron R. CurrieAbstract:Abstract Leaf-Cutting Ants are one of the mai
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interaction between workers during a short time window is required for bacterial symbiont transmission in acromyrmex leaf cutting Ants
PLOS ONE, 2014Co-Authors: Sarah E Marsh, Michael Poulsen, Cameron R. Currie, Adrian A PintotomasAbstract:Stable associations between partners over time are critical for the evolution of mutualism. Hosts employ a variety of mechanisms to maintain specificity with bacterial associates. Acromyrmex Leaf-Cutting Ants farm a fungal cultivar as their primary nutrient source. These Ants also carry a Pseudonocardia Actinobacteria exosymbiont on their bodies that produces antifungal compounds that help inhibit specialized parasites of the Ants' fungal garden. Major workers emerge from their pupal cases (eclose) symbiont-free, but exhibit visible Actinobacterial coverage within 14 days post-eclosion. Using subcolony experiments, we investigate exosymbiont transmission within Acromyrmex colonies. We found successful transmission to newly eclosed major workers fostered by major workers with visible Actinobacteria in all cases (100% acquiring, n=19). In contrast, newly eclosed major workers reared without exosymbiont-carrying major workers did not acquire visible Actinobacteria (0% acquiring, n=73). We further show that the majority of Ants exposed to major workers with exosymbionts within 2 hours of eclosion acquired bacteria (60.7% acquiring, n=28), while normal acquisition did not occur when exposure occurred later than 2 hours post-eclosion (0% acquiring, n=18). Our findings show that transmission of exosymbionts to newly eclosed major workers occurs through interactions with exosymbiont-covered workers within a narrow time window after eclosion. This mode of transmission likely helps ensure the defensive function within colonies, as well as specificity and partner fidelity in the ant-bacterium association.
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caste specialization in behavioral defenses against fungus garden parasites in acromyrmex octospinosus leaf cutting Ants
Insectes Sociaux, 2011Co-Authors: D Abramowski, Cameron R. Currie, Michael PoulsenAbstract:Division of labor and caste specialization plays an important role in many aspects of social insect colony organization, including parasite defense. Within Leaf-Cutting ant colonies, worker caste specialization permeates colony tasks ranging from foraging, substrate incorporation, brood care, and chemical defenses via glandular secretions and mutualistic bacteria. Leaf-Cutting Ants rely on protecting a mutualistic fungus they grow for food from microfungi in the genus Escovopsis that parasitizes the ant–fungus relationship. Here, we examine whether Acromyrmex octospinosus leaf-cutter ant castes (minors and majors) display task specialization in two behavioral defenses against Escovopsis: fungus grooming (the removal of Escovopsis spores) and weeding (the removal of large pieces of Escovopsis-infected fungus garden). Using behavioral observations, we show that minors are the primary caste that performs fungus grooming, while weeding is almost exclusively performed by majors. In addition, using a sub-colony infection experimental setup, we show that at the early stages of infection, minors more efficiently remove Escovopsis spores from the fungus garden, thereby restricting Escovopsis spore germination and growth. At later stages of infection, after Escovopsis spore germination, we find that major workers are as efficient as minors in defending the fungus garden, likely due to the increased importance of weeding. Finally, we show, using SEM imaging, that the number of sensory structures is similar between minor and major workers. If these structures are invoked in recognition of the parasites, this finding suggests that both castes are able to sense Escovopsis. Our findings support that leaf-cutter ant behavioral defense tasks against Escovopsis are subject to caste specialization, likely facilitated by worker sizes being optimal for grooming and weeding by minors and majors, respectively, with important consequences for cultivar defense.
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The role of symbiont genetic distance and potential adaptability in host preference towards Pseudonocardia symbionts in Acromyrmex Leaf-Cutting Ants.
Journal of insect science (Online), 2011Co-Authors: Michael Poulsen, Janielle Maynard, Damien L Roland, Cameron R. CurrieAbstract:Fungus-growing Ants display symbiont preference in behavioral assays, both towards the fungus they cultivate for food and Actinobacteria they maintain on their cuticle for antibiotic production against parasites. These Actinobacteria, genus Pseudonocardia Henssen (Pseudonocardiacea: Actinomycetales), help defend the Ants' fungal mutualist from specialized parasites. In Acromyrmex Mayr (Hymenoptera: Formicidae) Leaf-Cutting Ants, individual colonies maintain either a single or a few strains of Pseudonocardia, and the symbiont is primarily vertically transmitted between generations by colony-founding queens. A recent report found that Acromyrmex workers are able to differentiate between their native Pseudonocardia strain and non-native strains isolated from sympatric or allopatric Acromyrmex species, and show preference for their native strain. Here we explore worker preference when presented with two non-native strains, elucidating the role of genetic distance on preference between strains and Pseudonocardia origin. Our findings suggest that Ants tend to prefer bacteria more closely related to their native bacterium and that genetic similarity is probably more important than whether symbionts are ant-associated or free-living. Preliminary findings suggest that when continued exposure to a novel Pseudonocardia strain occurs, ant symbiont preference is potentially adaptable, with colonies apparently being able to alter symbiont preference over time. These findings are discussed in relation to the role of adaptive recognition, potential ecological flexibility in symbiont preference, and more broadly, in relation to self versus non-self recognition.
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variation in pseudonocardia antibiotic defence helps govern parasite induced morbidity in acromyrmex leaf cutting Ants
Environmental Microbiology Reports, 2009Co-Authors: Michael Poulsen, Matías J. Cafaro, Ainslie E. F. Little, Nicole M. Gerardo, Daniel P Erhardt, Brad Tebbets, Bruce S Klein, Cameron R. CurrieAbstract:Summary Host–parasite associations are potentially shaped by evolutionary reciprocal selection dynamics, in which parasites evolve to overcome host defences and hosts are selected to counteract these through the evolution of new defences. This is expected to result in variation in parasite-defence interactions, and the evolution of resistant parasites causing increased virulence. Fungus-growing Ants maintain antibioticproducing Pseudonocardia (Actinobacteria) that aid in protection against specialized parasites of the Ants’ fungal gardens, and current evidence indicates that both symbionts have been associated with the Ants for millions of years. Here we examine the extent of variation in the defensive capabilities of the ant–actinobacterial association against Escovopsis (parasite-defence interactions), and evaluate how variation impacts colonies of fungus-growing Ants. We focus on five species of Acromyrmex Leaf-Cutting Ants, crossing 12 strains of Pseudonocardia with 12 strains of Escovopsis in a Petri plate bioassay experiment, and subsequently conduct subcolony infection experiments using resistant and non-resistant parasite strains. Diversity in parasite-defence interactions, including pairings where the parasites are resistant, suggests that chemical variation in the antibiotics produced by different actinobacterial strains are responsible for the observed variation in parasite susceptibility. We evaluate the role this variation plays showing that infection of ant subcolonies with resistant parasite strains results in significantly higher parasite-induced morbidity with respect to garden biomass loss. Our findings thus further establish the role of Pseudonocardia-derived antibiotics in helping defend the Ants’ fungus garden from the parasite Escovopsis, and provide evidence that small molecules can play important roles as antibiotics in a natural system.
