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      Macronutrients modulate survival to infection and immunity in Drosophila

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          Abstract

          1. Immunity and nutrition are two essential modulators of individual fitness. However, while the implications of immune function and nutrition on an individual's lifespan and reproduction are well established, the interplay between feeding behaviour, infection and immune function remains poorly understood. Asking how ecological and physiological factors affect immune responses and resistance to infections is a central theme of eco‐immunology.

          2. In this study, we used the fruit fly, Drosophila melanogaster, to investigate how infection through septic injury modulates nutritional intake and how macronutrient balance affects survival to infection by the pathogenic Gram‐positive bacterium Micrococcus luteus.

          3. Our results show that infected flies maintain carbohydrate intake, but reduce protein intake, thereby shifting from a protein‐to‐carbohydrate (P:C) ratio of ~1:4 to ~1:10 relative to non‐infected and sham‐infected flies. Strikingly, the proportion of flies dying after M. luteus infection was significantly lower when flies were fed a low‐P high‐C diet, revealing that flies shift their macronutrient intake as means of nutritional self‐medication against bacterial infection.

          4. These results are likely due to the effects of the macronutrient balance on the regulation of the constitutive expression of innate immune genes, as a low‐P high‐C diet was linked to an upregulation in the expression of key antimicrobial peptides.

          5. Together, our results reveal the intricate relationship between macronutrient intake and resistance to infection and integrate the molecular cross‐talk between metabolic and immune pathways into the framework of nutritional immunology.

          Abstract

          Self‐medication has been traditionally seen as animals using molecules such as secondary plant compounds or other non‐nutritive substances with antiparasitic activity. The authors' results support that self‐medication can happen through modulating dietary macronutrient selection to stimulate immunity and compensate for the negative effects of the infection on fitness traits.

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          Most cited references59

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          Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology

          In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.
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            State-dependent life histories.

            Life-history theory is concerned with strategic decisions over an organism's lifetime. Evidence is accumulating about the way in which these decisions depend on the organism's physiological state and other components such as external circumstances. Phenotypic plasticity may be interpreted as an organism's response to its state. The quality of offspring may depend on the state and behaviour of the mother. Recent theoretical advances allow these and other state-dependent effects to be modelled within the same framework.
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              Tolerance of infections.

              A host has two methods to defend against pathogens: It can clear the pathogens or reduce their impact on health in other ways. The first, resistance, is well studied. Study of the second, which ecologists call tolerance, is in its infancy. Tolerance measures the dose response curve of a host's health in reaction to a pathogen and can be studied in a simple quantitative manner. Such studies hold promise because they point to methods of treating infections that put evolutionary pressures on microbes different from antibiotics and vaccines. Studies of tolerance will provide an improved foundation to describe our interactions with all microbes: pathogenic, commensal, and mutualistic. One obvious mechanism affecting tolerance is the intensity of an immune response; an overly exuberant immune response can cause collateral damage through immune effectors and because of the energy allocated away from other physiological functions. There are potentially many other tolerance mechanisms, and here we systematically describe tolerance using a variety of animal systems.
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                Author and article information

                Contributors
                fleur.ponton@mq.edu.au
                Journal
                J Anim Ecol
                J Anim Ecol
                10.1111/(ISSN)1365-2656
                JANE
                The Journal of Animal Ecology
                John Wiley and Sons Inc. (Hoboken )
                0021-8790
                1365-2656
                09 December 2019
                February 2020
                : 89
                : 2 ( doiID: 10.1111/jane.v89.2 )
                : 460-470
                Affiliations
                [ 1 ] Department of Biological Sciences Macquarie University Sydney NSW Australia
                [ 2 ] Charles Perkins Centre and School of Life and Environmental Sciences The University of Sydney Sydney NSW Australia
                [ 3 ] School of Life Sciences University of Lincoln Lincoln UK
                [ 4 ] Lancaster Environment Centre Lancaster University Lancaster UK
                Author notes
                [*] [* ] Correspondence

                Fleur Ponton

                Email: fleur.ponton@ 123456mq.edu.au

                Author information
                https://orcid.org/0000-0001-7156-3896
                https://orcid.org/0000-0003-3561-1920
                https://orcid.org/0000-0002-3801-8316
                https://orcid.org/0000-0001-5264-6522
                https://orcid.org/0000-0003-0256-7687
                Article
                JANE13126
                10.1111/1365-2656.13126
                7027473
                31658371
                2a4679b0-d8ed-4c98-a53c-71b7e72ead2e
                © 2019 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society

                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
                : 12 February 2019
                : 17 July 2019
                Page count
                Figures: 5, Tables: 0, Pages: 11, Words: 8255
                Funding
                Funded by: Australian Research Council , open-funder-registry 10.13039/501100000923;
                Award ID: DP130103222
                Funded by: Macquarie University , open-funder-registry 10.13039/501100001230;
                Award ID: 38277130
                Categories
                Research Article
                Physiological Ecology
                Custom metadata
                2.0
                February 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.5 mode:remove_FC converted:18.02.2020

                Ecology
                drosophila,immunity,infection,macronutrients,nutrition
                Ecology
                drosophila, immunity, infection, macronutrients, nutrition

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