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      Community context for mechanisms of disease dilution: insights from linking epidemiology and plant–soil feedback theory

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          Abstract

          In many natural systems, diverse host communities can reduce disease risk, though less is known about the mechanisms driving this “dilution effect.” We relate feedback theory, which focuses on pathogen‐mediated coexistence, to mechanisms of dilution derived from epidemiological models, with the central goal of gaining insights into host–pathogen interactions in a community context. We first compare the origin, structure, and application of epidemiological and feedback models. We then explore the mechanisms of dilution, which are grounded in single‐pathogen, single‐host epidemiological models, from the perspective of feedback theory. We also draw on feedback theory to examine how coinfecting pathogens, and pathogens that vary along a host specialist–generalist continuum, apply to dilution theory. By identifying synergies among the feedback and epidemiological approaches, we reveal ways in which organisms occupying different trophic levels contribute to diversity–disease relationships. Additionally, using feedbacks to distinguish dilution in disease incidence from dilution in the net effect of disease on host fitness allows us to articulate conditions under which definitions of dilution may not align. After ascribing dilution mechanisms to macro‐ or microorganisms, we propose ways in which each contributes to diversity–disease and productivity–diversity relationships. Our analyses lead to predictions that can guide future research efforts.

          Abstract

          In many natural systems, diverse host communities can reduce disease risk, though less is known about the mechanisms driving this “dilution effect.” We relate feedback theory, which focuses on pathogen‐mediated coexistence, to mechanisms of dilution derived from epidemiological models, with the central goal of gaining insights into host–pathogen interactions in a community context.

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          Most cited references108

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          Induced systemic resistance by beneficial microbes.

          Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
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            Predation, apparent competition, and the structure of prey communities

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                Author and article information

                Contributors
                ccollins@bard.edu
                Journal
                Ann N Y Acad Sci
                Ann. N. Y. Acad. Sci
                10.1111/(ISSN)1749-6632
                NYAS
                Annals of the New York Academy of Sciences
                John Wiley and Sons Inc. (Hoboken )
                0077-8923
                1749-6632
                13 March 2020
                June 2020
                : 1469
                : 1 , The Year in Ecology and Conservation Biology ( doiID: 10.1111/nyas.v1469.1 )
                : 65-85
                Affiliations
                [ 1 ] Biology Program Bard College Annandale‐on‐Hudson New York
                [ 2 ] Department of Ecology and Evolutionary Biology University of Kansas Lawrence Kansas
                [ 3 ] Kansas Biological Survey University of Kansas Lawrence Kansas
                [ 4 ] Department of Biology Sarah Lawrence College Bronxville New York
                Author notes
                [*] [* ]Address for correspondence: Cathy D. Collins, Biology Program, Bard College, 30 Campus Rd Annandale, Annandale‐on‐Hudson, NY 12504‐5000. ccollins@ 123456bard.edu

                Author information
                https://orcid.org/0000-0002-7205-7247
                https://orcid.org/0000-0003-4068-3582
                https://orcid.org/0000-0003-1174-7575
                Article
                NYAS14325
                10.1111/nyas.14325
                7317922
                32170775
                53929972-2aca-482d-8726-fed7a2957a3f
                © 2020 The Authors. Annals of the New York Academy of Sciences published by Wiley Periodicals, Inc. on behalf of New York Academy of Sciences

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 02 November 2019
                : 31 January 2020
                : 13 February 2020
                Page count
                Figures: 6, Tables: 1, Pages: 21, Words: 13008
                Funding
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: DEB‐1655972
                Award ID: DEB‐1655893
                Award ID: DEB‐1738041
                Award ID: OIA 1656006
                Categories
                Nyasecol9119
                Nyasevol2572
                Nyasmicr2050
                Nyaspubl8657
                Review
                Reviews
                Custom metadata
                2.0
                June 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.4 mode:remove_FC converted:26.06.2020

                Uncategorized
                species coexistence,pathogen,dilution effect,disease ecology,feedbacks,trophic interactions

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