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      Repeated Evolution of Fungal Cultivar Specificity in Independently Evolved Ant-Plant-Fungus Symbioses

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          Abstract

          Some tropical plant species possess hollow structures (domatia) occupied by ants that protect the plant and in some cases also provide it with nutrients. Most plant-ants tend patches of chaetothyrialean fungi within domatia. In a few systems it has been shown that the ants manure the fungal patches and use them as a food source, indicating agricultural practices. However, the identity of these fungi has been investigated only in a few samples. To examine the specificity and constancy of ant-plant-fungus interactions we characterised the content of fungal patches in an extensive sampling of three ant-plant symbioses ( Petalomyrmex phylax/ Leonardoxa africana subsp. africana, Aphomomyrmex afer/ Leonardoxa africana subsp. letouzeyi and Tetraponera aethiops/ Barteria fistulosa) by sequencing the Internal Transcribed Spacers of ribosomal DNA. For each system the content of fungal patches was constant over individuals and populations. Each symbiosis was associated with a specific, dominant, primary fungal taxon, and to a lesser extent, with one or two specific secondary taxa, all of the order Chaetothyriales. A single fungal patch sometimes contained both a primary and a secondary taxon. In one system, two founding queens were found with the primary fungal taxon only, one that was shown in a previous study to be consumed preferentially. Because the different ant-plant symbioses studied have evolved independently, the high specificity and constancy we observed in the composition of the fungal patches have evolved repeatedly. Specificity and constancy also characterize other cases of agriculture by insects.

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          Non-random coextinctions in phylogenetically structured mutualistic networks.

          The interactions between plants and their animal pollinators and seed dispersers have moulded much of Earth's biodiversity. Recently, it has been shown that these mutually beneficial interactions form complex networks with a well-defined architecture that may contribute to biodiversity persistence. Little is known, however, about which ecological and evolutionary processes generate these network patterns. Here we use phylogenetic methods to show that the phylogenetic relationships of species predict the number of interactions they exhibit in more than one-third of the networks, and the identity of the species with which they interact in about half of the networks. As a consequence of the phylogenetic effects on interaction patterns, simulated extinction events tend to trigger coextinction cascades of related species. This results in a non-random pruning of the evolutionary tree and a more pronounced loss of taxonomic diversity than expected in the absence of a phylogenetic signal. Our results emphasize how the simultaneous consideration of phylogenetic information and network architecture can contribute to our understanding of the structure and fate of species-rich communities.
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            Uniting pattern and process in plant-animal mutualistic networks: a review.

            Ecologists and evolutionary biologists are becoming increasingly interested in networks as a framework to study plant-animal mutualisms within their ecological context. Although such focus on networks has brought about important insights into the structure of these interactions, relatively little is still known about the mechanisms behind these patterns. The aim in this paper is to offer an overview of the mechanisms influencing the structure of plant-animal mutualistic networks. A brief summary is presented of the salient network patterns, the potential mechanisms are discussed and the studies that have evaluated them are reviewed. This review shows that researchers of plant-animal mutualisms have made substantial progress in the understanding of the processes behind the patterns observed in mutualistic networks. At the same time, we are still far from a thorough, integrative mechanistic understanding. We close with specific suggestions for directions of future research, which include developing methods to evaluate the relative importance of mechanisms influencing network patterns and focusing research efforts on selected representative study systems throughout the world.
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              The evolution of fungus-growing termites and their mutualistic fungal symbionts.

              We have estimated phylogenies of fungus-growing termites and their associated mutualistic fungi of the genus Termitomyces using Bayesian analyses of DNA sequences. Our study shows that the symbiosis has a single African origin and that secondary domestication of other fungi or reversal of mutualistic fungi to a free-living state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite species can have different symbionts. Data are consistent with horizontal transmission of fungal symbionts in both the ancestral state of the mutualism and most of the extant taxa. Clonal vertical transmission of fungi, previously shown to be common in the genus Microtermes (via females) and in the species Macrotermes bellicosus (via males) [Johnson, R. A., Thomas, R. J., Wood, T. G. & Swift, M. J. (1981) J. Nat. Hist. 15, 751-756], is derived with two independent origins. Despite repeated host switching, statistical tests taking phylogenetic uncertainty into account show a significant congruence between the termite and fungal phylogenies, because mutualistic interactions at higher taxonomic levels show considerable specificity. We identify common characteristics of fungus-farming evolution in termites and ants, which apply despite the major differences between these two insect agricultural systems. We hypothesize that biparental colony founding may have constrained the evolution of vertical symbiont transmission in termites but not in ants where males die after mating.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                25 July 2013
                : 8
                : 7
                : e68101
                Affiliations
                [1 ]Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), CNRS/CIRAD-Bios/Université Montpellier 2, Montpellier, France
                [2 ]Institut Universitaire de France, Montpellier, France
                [3 ]Département de Biologie, Université des Sciences et Techniques de Masuku (USTM), Franceville, Gabon
                [4 ]Laboratory of Zoology, University of Yaoundé I, Yaoundé, Cameroun
                Emory University, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: RB CB DM CA CDL. Performed the experiments: RB SD ASL CB LB CDL. Analyzed the data: RB SD ASL CB LB. Wrote the paper: RB CB DM.

                Article
                PONE-D-13-09161
                10.1371/journal.pone.0068101
                3723801
                23935854
                020fb102-1cf2-40ff-952b-411e2ab69245
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 March 2013
                : 24 May 2013
                Page count
                Pages: 9
                Funding
                This project was supported by the network “Bibliothèque du Vivant” ( http://bdv.ups-tlse.fr/), funded by the CNRS, the Muséum National d'Histoire Naturelle, the INRA and the CEA (Centre National de Séquençage). It was also funded by grants to R. Blatrix and D. McKey from three programmes of the French Agence Nationale de la Recherche ( www.agence-nationale-recherche.fr): “Young scientists” (research agreement no. ANR-06-JCJC-0127), “Biodiversity” (IFORA project) and “Sixth extinction” (C3A project). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Species Interactions
                Biodiversity
                Evolutionary Ecology
                Microbial Ecology
                Population Ecology
                Evolutionary Biology
                Evolutionary Processes
                Coevolution
                Evolutionary Systematics
                Taxonomy
                Microbial Taxonomy
                Forms of Evolution
                Coevolution
                Convergent Evolution
                Evolutionary Ecology
                Microbiology
                Mycology
                Fungal Evolution
                Fungi

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                Uncategorized

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