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      Extreme Competence: Keystone Hosts of Infections

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          Abstract

          Individual hosts differ extensively in their competence for parasites, but traditional research has discounted this variation, partly because modeling such heterogeneity is difficult. This discounting has diminished as tools have improved and recognition has grown that some hosts, the extremely competent, can have exceptional impacts on disease dynamics. Most prominent among these hosts are the superspreaders, but other forms of extreme competence (EC) exist and others await discovery; each with potentially strong but distinct implications for disease emergence and spread. Here, we propose a framework for the study and discovery of EC, suitable for different host–parasite systems, which we hope enhances our understanding of how parasites circulate and evolve in host communities.

          Highlights

          A few members of host populations, so-called superspreaders, have disproportionate impacts on the risk of infectious disease emergence and spread.

          Several other forms of EC exist; some of which might be exceptionally protective.

          To discover and understand forms of EC, it is imperative to describe the distribution of, and covariation among, traits of individual hosts that mediate the many stages of host–parasite interactions.

          Here, we provide a framework to do so, emphasizing how interplay among host traits related to parasite exposure behavior, susceptibility, replicability of parasites on/in hosts, and transmissibility, comprise host competence.

          We hope this framework helps reveal new forms of EC and informs and improves management of disease risk.

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          Most cited references58

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          Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

          From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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            The silent threat: asymptomatic parasitemia and malaria transmission.

            Scale-up of malaria control interventions has resulted in a substantial decline in global malaria morbidity and mortality. Despite this achievement, there is evidence that current interventions alone will not lead to malaria elimination in most malaria-endemic areas and additional strategies need to be considered. Use of antimalarial drugs to target the reservoir of malaria infection is an option to reduce the transmission of malaria between humans and mosquito vectors. However, a large proportion of human malaria infections are asymptomatic, requiring treatment that is not triggered by care-seeking for clinical illness. This article reviews the evidence that asymptomatic malaria infection plays an important role in malaria transmission and that interventions to target this parasite reservoir may be needed to achieve malaria elimination in both low- and high-transmission areas.
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              Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation.

              The mammalian intestine is colonized by beneficial commensal bacteria and is a site of infection by pathogens, including helminth parasites. Helminths induce potent immunomodulatory effects, but whether these effects are mediated by direct regulation of host immunity or indirectly through eliciting changes in the microbiota is unknown. We tested this in the context of virus-helminth coinfection. Helminth coinfection resulted in impaired antiviral immunity and was associated with changes in the microbiota and STAT6-dependent helminth-induced alternative activation of macrophages. Notably, helminth-induced impairment of antiviral immunity was evident in germ-free mice, but neutralization of Ym1, a chitinase-like molecule that is associated with alternatively activated macrophages, could partially restore antiviral immunity. These data indicate that helminth-induced immunomodulation occurs independently of changes in the microbiota but is dependent on Ym1. Copyright © 2014, American Association for the Advancement of Science.
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                Author and article information

                Contributors
                Journal
                Trends Ecol Evol
                Trends Ecol. Evol. (Amst.)
                Trends in Ecology & Evolution
                Elsevier Ltd.
                0169-5347
                1872-8383
                29 January 2019
                April 2019
                29 January 2019
                : 34
                : 4
                : 303-314
                Affiliations
                [1 ]Global and Planetary Health, University of South Florida, Tampa, Florida 33620, USA
                [2 ]School of Biological Sciences, Monash University, VIC 3800, Australia
                [3 ]School of Life and Environmental Sciences, Deakin University, Geelong Waurn Ponds, VIC 3216, Australia
                [4 ]Menzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7008, Australia
                [5 ]School of Natural Sciences, University of Tasmania, Hobart, TAS 7001, Australia
                [6 ]Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
                [7 ]School of Science and Health, Western Sydney University, Penrith, NSW 2751, Australia
                [8 ]Environmental Futures Research Institute, Griffith University, Nathan, QLD 4111, Australia
                [9 ]School of Biological, Earth and Environmental Sciences, Evolution & Ecology Research Centre, University of New South Wales, Sydney, NSW 2052, Australia
                [10 ]School of Life and Environmental Sciences (SOLES), University of Sydney, Sydney, NSW 2006, Australia
                [11 ]Institute of Ecology and Biodiversity, Universidad de Chile, Santiago, Chile
                [12 ]CSIRO Health & Biosecurity at the Australian Animal Health Laboratory, Geelong, VIC 3220, Australia
                Author notes
                Article
                S0169-5347(18)30301-X
                10.1016/j.tree.2018.12.009
                7114649
                30704782
                b229b95a-1923-420c-b226-5a59479aa1d2
                © 2018 Elsevier Ltd. All rights reserved.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

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                Categories
                Article

                Ecology
                disease,epidemic,infection,zoonosis
                Ecology
                disease, epidemic, infection, zoonosis

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