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      The sudden emergence of pathogenicity in insect–fungus symbioses threatens naive forest ecosystems

      1 , 2 , 1
      Proceedings of the Royal Society B: Biological Sciences
      The Royal Society

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          Abstract

          Invasive symbioses between wood-boring insects and fungi are emerging as a new and currently uncontrollable threat to forest ecosystems, as well as fruit and timber industries throughout the world. The bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae) constitute the large majority of these pests, and are accompanied by a diverse community of fungal symbionts. Increasingly, some invasive symbioses are shifting from non-pathogenic saprotrophy in native ranges to a prolific tree-killing in invaded ranges, and are causing significant damage. In this paper, we review the current understanding of invasive insect–fungus symbioses. We then ask why some symbioses that evolved as non-pathogenic saprotrophs, turn into major tree-killers in non-native regions. We argue that a purely pathology-centred view of the guild is not sufficient for explaining the lethal encounters between exotic symbionts and naive trees. Instead, we propose several testable hypotheses that, if correct, lead to the conclusion that the sudden emergence of pathogenicity is a new evolutionary phenomenon with global biogeographical dynamics. To date, evidence suggests that virulence of the symbioses in invaded ranges is often triggered when several factors coincide: (i) invasion into territories with naive trees, (ii) the ability of the fungus to either overcome resistance of the naive host or trigger a suicidal over-reaction, and (iii) an ‘olfactory mismatch’ in the insect whereby a subset of live trees is perceived as dead and suitable for colonization. We suggest that individual cases of tree mortality caused by invasive insect–fungus symbionts should no longer be studied separately, but in a global, biogeographically and phylogenetically explicit comparative framework.

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          Most cited references45

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          Interactions among Scolytid bark beetles, their associated fungi, and live host conifers.

          Scolytid bark beetles that colonize living conifers are frequently associated with specific fungi that are carried in specialized structures or on the body surface. These fungi are introduced into the tree during the attack process. The continuing association suggests that there is mutual benefit to the fitness of both beetles and fungi. The fungal species may benefit from the association with the beetles by transport to new host trees. Beetle species may benefit from the association with fungi by feeding on the fungi, or by the fungi contributing to the death of the host trees through mycelial penetration of host tissue, toxin release, interactions with preformed and induced conifer defenses, or the combined action of both beetles and fungi during colonization. Extensive research has been directed towards characterizing the interactions of beetle-fungal complexes with live host conifers and determining the ecological advantages for maintaining the associations. However, differences among systems and how species interact under different population and environmental conditions make it difficult to generalize about the importance of the separate biological components in successful host colonization.
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            Historical Accumulation of Nonindigenous Forest Pests in the Continental United States

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              Low host specificity of herbivorous insects in a tropical forest.

              Two decades of research have not established whether tropical insect herbivores are dominated by specialists or generalists. This impedes our understanding of species coexistence in diverse rainforest communities. Host specificity and species richness of tropical insects are also key parameters in mapping global patterns of biodiversity. Here we analyse data for over 900 herbivorous species feeding on 51 plant species in New Guinea and show that most herbivorous species feed on several closely related plant species. Because species-rich genera are dominant in tropical floras, monophagous herbivores are probably rare in tropical forests. Furthermore, even between phylogenetically distant hosts, herbivore communities typically shared a third of their species. These results do not support the classical view that the coexistence of herbivorous species in the tropics is a consequence of finely divided plant resources; non-equilibrium models of tropical diversity should instead be considered. Low host specificity of tropical herbivores reduces global estimates of arthropod diversity from 31 million (ref. 1) to 4 6 million species. This finding agrees with estimates based on taxonomic collections, reconciling an order of magnitude discrepancy between extrapolations of global diversity based on ecological samples of tropical communities with those based on sampling regional faunas.
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                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B.
                The Royal Society
                0962-8452
                1471-2954
                October 07 2011
                July 13 2011
                October 07 2011
                : 278
                : 1720
                : 2866-2873
                Affiliations
                [1 ]Department of Biology and Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC 27695, USA
                [2 ]North Carolina Cooperative Fish and Wildlife Research Unit, North Carolina State University, Raleigh, NC 27695, USA
                Article
                10.1098/rspb.2011.1130
                21752822
                2e4f6b64-449f-4135-9df9-31bb329db045
                © 2011

                https://royalsociety.org/journals/ethics-policies/data-sharing-mining/

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