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Jacobus J. Boomsma - One of the best experts on this subject based on the ideXlab platform.
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Diversity and Transmission of Gut Bacteria in Atta and Acromyrmex Leaf-Cutting Ants during Development.
Frontiers in microbiology, 2017Co-Authors: Mariya Zhukova, Morten Schiøtt, Panagiotis Sapountzis, Jacobus J. BoomsmaAbstract:The social Hymenoptera have distinct larval and adult stages separated by metamorphosis, which implies striking remodeling of external and internal body structures during the pupal stage. This imposes challenges to gut symbionts as existing cultures are lost and may or may not need to be replaced. To elucidate the extent to which metamorphosis interrupts associations between bacteria and hosts, we analysed changes in gut microbiota during development and traced the transmission routes of dominant symbionts from the egg to adult stage in the leaf-cutting ants Acromyrmex echinatior and Atta cephalotes, which are both important functional herbivores in the New World tropics. Bacterial density remained similar across the developmental stages of Acromyrmex, but Atta brood had very low bacterial prevalences suggesting that bacterial gut symbionts are not actively maintained. We found that Wolbachia was the absolute dominant bacterial species across developmental stages in Acromyrmex and we confirmed that Atta lacks Wolbachia also in the immature stages, and had mostly Mollicutes bacteria in the adult worker guts. Wolbachia in Acromyrmex appeared to be transovarially transmitted similar to transmission in solitary insects. In contrast, Mollicutes were socially transmitted from old workers to newly emerged callows. We found that larval and pupal guts of both ant species contained Pseudomonas and Enterobacter bacteria that are also found in fungus gardens, but hardly or not in adult workers, suggesting they are beneficial only for larval growth and development. Our results reveal that transmission pathways for bacterial symbionts may be very different both between developmental stages and between sister genera and that identifying the mechanisms of bacterial acquisition and loss will be important to clarify their putative mutualistic functions.
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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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EPHEMERAL WINDOWS OF OPPORTUNITY FOR HORIZONTAL TRANSMISSION OF FUNGAL SYMBIONTS IN LEAF-CUTTING ANTS
Evolution; international journal of organic evolution, 2009Co-Authors: Michael Poulsen, Hermógenes Fernández-marín, Cameron R. Currie, Jacobus J. BoomsmaAbstract:Evolutionary theory predicts that hosts are selected to prevent mixing of genetically different symbionts when competition among lineages reduces the productivity of a mutualism. The symbionts themselves may also defend their interests: recent studies of Acromyrmex leaf-cutting ants showed that somatic incompatibility enforces single-clone gardens within mature colonies, thereby constraining horizontal transmission of fungal symbionts. However, phylogenetic analyses indicate that symbiont switches occur frequently enough to remove most signs of host-symbiont cocladogenesis. Here we resolve this paradox by showing that transmission among newly founded Acromyrmex colonies is not constrained. All tested queens of sympatric A. octospinosus and A. echinatior offered a novel fragment of fungus garden accepted the new symbiont. The outcome was unaffected by genetic distance between the novel and the original symbiont, and by the ant species the novel symbiont came from. The colony founding stage may thus provide an efficient but transient window for horizontal transmission, in which the fungus is unable to actively defend its partnership position before the host feeds on it, so that host fecal droplets remain compatible with alternative strains during the early stage of colony founding. We discuss how brief stages of low commitment between partners may increase the evolutionary stability of ancient coevolved mutualisms.
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Chemical mimicry in an incipient leaf-cutting ant social parasite
Behavioral Ecology and Sociobiology, 2007Co-Authors: Duccio Lambardi, Stefano Turillazzi, Francesca R. Dani, Jacobus J. BoomsmaAbstract:Some social parasites of insect societies are known to use brute force when usurping a host colony, but most use more subtle forms of chemical cheating either by expressing as few recognition cues as possible to avoid being recognized or by producing similar recognition cues to the host to achieve positive discrimination. The former “chemical insignificance” strategy represents a more general adaptive syndrome than the latter “chemical mimicry” strategy and is expected to be characteristic of early evolutionary stages of social parasitism. We tested this hypothesis by experimentally analyzing the efficiency by which Acromyrmex echinatior leaf-cutting ants recognize intruding workers of the incipient social parasite Acromyrmex insinuator . The results were consistent with the parasite being “chemically insignificant” and not with the “chemical mimicry” hypothesis. Gas chromatography–mass spectrometry analysis of cuticular hydrocarbon profiles showed that social parasite workers produce significantly fewer hydrocarbons overall and that their typical profiles have very low amounts of hydrocarbons in the “normal” C29–C35 range but large quantities of unusually heavy C43–C45 hydrocarbons. This suggests that the C29–C35 hydrocarbons are instrumental in normal host nestmate recognition and that the C43–C45 compounds, all of which are dienes and thus more fluid than the corresponding saturated compounds, may reinforce “chemical insignificance” by blurring any remaining variation in recognition cues.
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Self-restraint and sterility in workers of Acromyrmex and Atta leafcutter ants
Insectes Sociaux, 2005Co-Authors: Michiel B. Dijkstra, David R. Nash, Jacobus J. BoomsmaAbstract:Queens of leafcutter ants (Acromyrmex and Atta) are highly multiply mated, resulting in a potential queenworker and worker-worker conflict over who should produce the males in the colony. We studied whether this conflict is expressed, by determining the amount of reproductive egg-laying by workers in queenright colonies of Acromyrmex echinatior, Acromyrmex octospinosus, Atta cephalotes, and Atta sexdens through ovary dissections. Worker sons are absent or rare in queenright Acromyrmex colonies, but can be produced in orphaned colonies. In Atta, most workers have rudimentary ovaries that never produce eggs, but a few (mostly small and medium workers that form a retinue around the queen) lay many trophic eggs for consumption by the queen. These eggs are large, flaccid, and lacking in yolk compared to queen-laid eggs, and appear to be always inviable. In Acromyrmex, many workers (especially young large workers) lay eggs that are similar in size to queen-laid eggs, but mostly with a reduced amount of yolk. Trophic eggs appear to be an important source of food for larvae in Acromyrmex (especially in Ac. echinatior), but not in Atta. Five (0.8) of 616 dissected Ac. echinatior workers but no Ac. octospinosus workers (n = 552), had ready-to-lay reproductive eggs. Old workers in all four species are incapable of laying eggs due to ovary resorption. We conclude that Atta workers are sterile, while Acromyrmex workers display reproductive self-restraint, possibly representing an earlier stage in the evolution towards worker sterility. Worker selfrestraint in Acromyrmex may be maintained by a queen or worker policing mechanism, but individual cost-benefit explanations may also apply.
Terezinha Maria Castro Della Lucia - One of the best experts on this subject based on the ideXlab platform.
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Immune Defense Strategies of Queens of the Social Parasite Ant Acromyrmex ameliae and Queens of Its Natural Hosts.
Neotropical entomology, 2021Co-Authors: Lailla C. Gandra, Danival José De Souza, Karina D. Amaral, Joel C. Couceiro, Rômulo A. C. Dângelo, Terezinha Maria Castro Della LuciaAbstract:Social parasitism is well known in ants, but many aspects of this social phenomenon remain mysterious and unexplored. In some cases, parasite queens, who are able to mate very rarely end up producing brood and, thus, depend virtually on the labor of host ants. In this work, we sought to test the occurrence of grooming by host workers of Acromyrmex subterraneus subterraneus Forel, to their own queens and queens of the parasite Acromyrmex ameliae De Souza, Soares and Della Lucia and to compare the immune defense responses of parasite queens and queens of A. subterraneus subterraneus and Acromyrmex subterraneus brunneus Forel, the natural hosts. Duration and frequency of behavioral acts were recorded. The relative size of the bulla and the encapsulation response to a standardized antigen were analyzed. Regarding behavioral acts, self-grooming (duration and frequency) and allogrooming (duration) were statistically different between the species; the first is more frequent and lasted longer in parasite queens, while the second act lasted longer in host ants than in parasite ants. The bulla of A. ameliae was approximately 50% wider than those of its hosts. Parasite queens exhibited a stronger immune response than host queens. The results of this work contribute to elucidate potential mechanisms involved in the parasitism capacity of A. ameliae queens such as their strategies of immune defense.
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Leaf-cutting ants in commercial forest plantations of Brazil: biological aspects and control methods
Southern Forests: a Journal of Forest Science, 2020Co-Authors: Germano Lopes Vinha, Pedro Guilherme Lemes, Ricardo Alcántara-de La Cruz, Terezinha Maria Castro Della Lucia, Carlos Frederico Wilcken, Edson Dias Da Silva, José Cola ZanuncioAbstract:Forest plantations represent the fourth largest crop by planted area in Brazil. However, leaf-cutting ants can compromise their establishment and development. Atta and Acromyrmex (Hymenoptera: Form...
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Actinomycetes inhibit filamentous fungi from the cuticle of Acromyrmex leafcutter ants.
Journal of basic microbiology, 2016Co-Authors: Rômulo Augusto Cotta Dângelo, Danival José De Souza, T. D. Mendes, Joel Da Cruz Couceiro, Terezinha Maria Castro Della LuciaAbstract:Actinomycetes bacteria associated with leafcutter ants produce secondary metabolites with antimicrobial properties against Escovopsis, a fungus specialized in attacking the gardens of fungus-growing ants, which denies the ants their food source. Because previous studies have used fungi isolated from fungus gardens but not from ant integument, the aims of the present study were to isolate actinomycetes associated with the cuticle of the Acromyrmex spp. and to quantify their inhibition abilities against the filamentous fungal species carried by these ants. The results demonstrated that actinomycetes had varied strain-dependent effects on several filamentous fungal species in addition to antagonistic activity against Escovopsis. The strain isolated from Acromyrmex balzani was identified as a Streptomyces species, whereas the remaining isolates were identified as different strains belonging to the genus Pseudonocardia. These findings corroborate the hypothesis that actinomycetes do not act specifically against Escovopsis mycoparasites and may have the ability to inhibit other species of pathogenic fungi.
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Recognition and Aggression of conspecific and heterospecific worker in Acromyrmex subterraneus subterraneus (Forel) (Hymenoptera: Formicidae)
Sociobiology, 2015Co-Authors: Tiago Georg Pikart, Pedro Guilherme Lemes, José Cola Zanuncio, Wagner Calixto De Castro Morais, Terezinha Maria Castro Della LuciaAbstract:Aggressive behavior is important for social insects because it makes possible for the colony to defend itself and the offspring from the action of invasive species. We studied the recognition and aggressiveness of the leaf-cutting ant Acromyrmex subterraneus subterraneus (Forel) to co-specific workers from other nest and heterospecific workers of Acromyrmex subterraneus molestans Santschi, Acromyrmex subterraneus brunneus (Forel) and Acromyrmex niger (Smith); and queens of their social parasite Acromyrmex ameliae De Souza, Soares and Della Lucia. Workers of other species were placed in contact with those of A. subterraneus subterraneus for three minutes and during this period the behavioral interactions were quantified. The aggressiveness index (AI) for each agonistic encounter was obtained. Acromyrmex subterraneus subterraneus workers exhibited greater aggressiveness against heterospecific than against conspecific competitors. Aggressiveness is connected to differences in the chemical profiles, which are larger in heterospecifics colonies.
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Consumo Foliar de Eucalyptus spp. por Acromyrmex disciger (Mayr, 1887) (Hymenoptera: Formicidae)
EntomoBrasilis, 2011Co-Authors: Wagner Calixto De Castro Morais, Norivaldo Dos Anjos, Terezinha Maria Castro Della LuciaAbstract:O potencial produtivo de plantios florestais e reduzido, dentre outros fatores, pela ocorrencia de pragas. No Brasil, as formigas-cortadeiras sao os principais insetos daninhos a cultura do eucalipto. Dentre as especies dessas formigas, Acromyrmex disciger (Mayr) se destaca na regiao Sudeste do Brasil. Entretanto, poucas sao as informacoes a respeito de seu potencial de dano as plantacoes de eucalipto. Este trabalho teve por objetivo quantificar o consumo foliar de eucalipto por A. disciger , em condicoes de laboratorio. Para isto, folhas frescas de Eucalyptus grandis W. Hill ex Maiden, Eucalyptus urophylla ST Blake e do hibrido E. urophylla x E. grandis foram oferecidas, com chance de escolha, a duas colonias de A. disciger , durante 24 horas, num total de oito repeticoes. O consumo foliar foi determinado pela diferenca entre as massas de folhas e de suas sobras, apos serem disponibilizadas as formigas. As operarias das duas colonias consumiram, respectivamente, 38,8 ± 3,2 g e 22,0 ± 2,3 g de folhas de eucalipto, por dia. Estes elevados valores podem sugerir estado de alerta para os danos que A. disciger pode causar nos plantios de eucalipto, merecendo, esta formiga-cortadeira, maior atencao. Eucalypt leaf-consumption by Acromyrmex disciger (Mayr) (Hymenoptera: Formicidae) Abstract. The productive potential of forest stands is reduced by pest occurrence among other factors. In Brazil, leaf-cutting ants are the most severe eucalypt pests. Acromyrmex disciger (Mayr) is prevalent in the south east Brazil. However, scarce information about its potential damage for Eucalyptus forests is available. This work deals to quantifying the eucalypt leaf-consumption by such specie of leaf-cutting ant. Fresh leaves were taken from trees of Eucalyptus grandis W. Hill ex Maiden, Eucalyptus urophylla ST Blake, and hybrid E. urophylla x E. grandis and served to different colonies of A. disciger , during 24 hours period, over eight different times. Leaf-consumption was calculated throughout fresh weights of leaves, before and after ants foraging. Each colony of A. disciger consumed 38.8 ± 3.2 g e 22.0 ± 2.3 g of eucalypt leaves, per day.
Fernando Luis Cônsoli - One of the best experts on this subject based on the ideXlab platform.
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Isolation and characterization of actinobacteria ectosymbionts from Acromyrmex subterraneus brunneus (Hymenoptera, Formicidae).
Microbiological research, 2010Co-Authors: Tiago Domingues Zucchi, Aline Sartori Guidolin, Fernando Luis CônsoliAbstract:Abstract The ectosymbiont actinobacterium Pseudonocardia was isolated from the integument of Acromyrmex leaf-cutter ants and seems to play a crucial role in maintaining asepsis of the nest. Currently, there has been an intensive search for Pseudonocardia associated with several attine species, but few studies have indicated that other actinobacteria may be associated with these ants as well. We therefore characterized the culturable actinobacteria community associated with the integument of the fungus-growing ant Acromyrmex subterraneus brunneus Forel, 1893 (Hymenoptera: Formicidae). Ectosymbionts were isolated using four different media and characterized by morphological and molecular (16S rDNA) methods. A total of 20 strains were isolated, of which 17 were characterized as Streptomyces spp., and one isolate each as Pseudonocardia, Kitassatospora and Propionicimonas. Unlike other Acromyrmex species, A. subterraneus brunneus is associated with a diversity of actinobacteria. Even though Pseudonocardia is present on this leaf-cutting ant’s integument, the number and diversity of Streptomyces spp. found differs from those of previous studies with other attine ants and suggest that different culturing approaches are needed to characterize the true diversity of microbes colonizing the integument of attine ants. Moreover, understanding the diversity of the culturable actinobacteria associated with A. subterraneus brunneus should increase our knowledge of the evolutionary relationship of this intricate symbiotic association.
Panagiotis Sapountzis - One of the best experts on this subject based on the ideXlab platform.
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Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?
Frontiers in microbiology, 2019Co-Authors: Sarah J. A. Tolley, Peter Nonacs, Panagiotis SapountzisAbstract:While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50-70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior, and its inquiline social parasite, Acromyrmex insinuator, and compare our results to a study published 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission.
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Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?
Frontiers Media S.A., 2019Co-Authors: Sarah J. A. Tolley, Peter Nonacs, Panagiotis SapountzisAbstract:While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50–70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior, and its inquiline social parasite, Acromyrmex insinuator, and compare our results to a study published more than 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission
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Table_1_Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?.pdf
2019Co-Authors: Sarah J. A. Tolley, Peter Nonacs, Panagiotis SapountzisAbstract:While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50–70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior, and its inquiline social parasite, Acromyrmex insinuator, and compare our results to a study published more than 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission.
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Image_1_Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?.TIFF
2019Co-Authors: Sarah J. A. Tolley, Peter Nonacs, Panagiotis SapountzisAbstract:While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50–70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior, and its inquiline social parasite, Acromyrmex insinuator, and compare our results to a study published more than 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission.
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Diversity and Transmission of Gut Bacteria in Atta and Acromyrmex Leaf-Cutting Ants during Development.
Frontiers in microbiology, 2017Co-Authors: Mariya Zhukova, Morten Schiøtt, Panagiotis Sapountzis, Jacobus J. BoomsmaAbstract:The social Hymenoptera have distinct larval and adult stages separated by metamorphosis, which implies striking remodeling of external and internal body structures during the pupal stage. This imposes challenges to gut symbionts as existing cultures are lost and may or may not need to be replaced. To elucidate the extent to which metamorphosis interrupts associations between bacteria and hosts, we analysed changes in gut microbiota during development and traced the transmission routes of dominant symbionts from the egg to adult stage in the leaf-cutting ants Acromyrmex echinatior and Atta cephalotes, which are both important functional herbivores in the New World tropics. Bacterial density remained similar across the developmental stages of Acromyrmex, but Atta brood had very low bacterial prevalences suggesting that bacterial gut symbionts are not actively maintained. We found that Wolbachia was the absolute dominant bacterial species across developmental stages in Acromyrmex and we confirmed that Atta lacks Wolbachia also in the immature stages, and had mostly Mollicutes bacteria in the adult worker guts. Wolbachia in Acromyrmex appeared to be transovarially transmitted similar to transmission in solitary insects. In contrast, Mollicutes were socially transmitted from old workers to newly emerged callows. We found that larval and pupal guts of both ant species contained Pseudomonas and Enterobacter bacteria that are also found in fungus gardens, but hardly or not in adult workers, suggesting they are beneficial only for larval growth and development. Our results reveal that transmission pathways for bacterial symbionts may be very different both between developmental stages and between sister genera and that identifying the mechanisms of bacterial acquisition and loss will be important to clarify their putative mutualistic functions.
Cameron R. Currie - One of the best experts on this subject based on the ideXlab platform.
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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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EPHEMERAL WINDOWS OF OPPORTUNITY FOR HORIZONTAL TRANSMISSION OF FUNGAL SYMBIONTS IN LEAF-CUTTING ANTS
Evolution; international journal of organic evolution, 2009Co-Authors: Michael Poulsen, Hermógenes Fernández-marín, Cameron R. Currie, Jacobus J. BoomsmaAbstract:Evolutionary theory predicts that hosts are selected to prevent mixing of genetically different symbionts when competition among lineages reduces the productivity of a mutualism. The symbionts themselves may also defend their interests: recent studies of Acromyrmex leaf-cutting ants showed that somatic incompatibility enforces single-clone gardens within mature colonies, thereby constraining horizontal transmission of fungal symbionts. However, phylogenetic analyses indicate that symbiont switches occur frequently enough to remove most signs of host-symbiont cocladogenesis. Here we resolve this paradox by showing that transmission among newly founded Acromyrmex colonies is not constrained. All tested queens of sympatric A. octospinosus and A. echinatior offered a novel fragment of fungus garden accepted the new symbiont. The outcome was unaffected by genetic distance between the novel and the original symbiont, and by the ant species the novel symbiont came from. The colony founding stage may thus provide an efficient but transient window for horizontal transmission, in which the fungus is unable to actively defend its partnership position before the host feeds on it, so that host fecal droplets remain compatible with alternative strains during the early stage of colony founding. We discuss how brief stages of low commitment between partners may increase the evolutionary stability of ancient coevolved mutualisms.
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Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants.
The ISME journal, 2007Co-Authors: Mingzi M Zhang, Michael Poulsen, Cameron R. CurrieAbstract:Symbiont choice has been proposed to play an important role in shaping many symbiotic relationships, including the fungus-growing ant-microbe mutualism. Over millions of years, fungus-growing ants have defended their fungus gardens from specialized parasites with antibiotics produced by an actinomycete bacterial mutualist (genus Pseudonocardia). Despite the potential of being infected by phylogenetically diverse strains of parasites, each ant colony maintains only a single Pseudonocardia symbiont strain, which is primarily vertically transmitted between colonies by the founding queens. In this study, we show that Acromyrmex leaf-cutter ants are able to differentiate between their native actinomycete strain and a variety of foreign strains isolated from sympatric and allopatric Acromyrmex species, in addition to strains originating from other fungus-growing ant genera. The recognition mechanism is sufficiently sensitive for the ants to discriminate between closely related symbiont strains. Our findings suggest that symbiont recognition may play a crucial role in the fungus-growing ant-bacterium mutualism, likely allowing the ants to retain ecological flexibility necessary for defending their garden from diverse parasites and, at the same time, resolve potential conflict that can arise from rearing competing symbiont strains.
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Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants.
Molecular ecology, 2005Co-Authors: Michael Poulsen, Jacobus J. Boomsma, Matías J. Cafaro, Cameron R. CurrieAbstract:Acromyrmex leaf-cutting ants maintain two highly specialized, vertically transmitted mutualistic ectosymbionts: basidiomycete fungi that are cultivated for food in under- ground gardens and actinomycete Pseudonocardia bacteria that are reared on the cuticle to produce antibiotics that suppress the growth of Escovopsis parasites of the fungus garden. Mutualism stability has been hypothesized to benefit from genetic uniformity of symbi- onts, as multiple coexisting strains are expected to compete and, thus, reduce the benefit of the symbiosis. However, the Pseudonocardia symbionts are likely to be involved in Red-Queen-like antagonistic co-evolution with Escovopsis so that multiple strains per host might be favoured by selection provided the cost of competition between bacterial strains is low. We examined the genetic uniformity of the Pseudonocardia symbionts of two sympat- ric species of Acromyrmex ants by comparing partial sequences of the nuclear Elongation Factor-Tu gene. We find no genetic variation in Pseudonocardia symbionts among nest mate workers, neither in Acromyrmex octospinosus , where colonies are founded by a single queen, nor in Acromyrmex echinatior , where mixing of bacterial lineages might happen when unrelated queens cofound a colony. We further show that the two ant species main- tain the same pool of Pseudonocardia symbionts, indicating that horizontal transmission occasionally occurs, and that this pool consists of two distinct clades of closely related Pseudonocardia strains. Our finding that individual colonies cultivate a single actinomycete strain is in agreement with predictions from evolutionary theory on host-symbiont conflict over symbiont mixing, but indicates that there may be constraints on the effectiveness of the bacterial symbionts on an evolutionary timescale.
