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      Effect of Juvenile Hormone on Resistance against Entomopathogenic Fungus Metarhizium robertsii Differs between Sexes

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          Abstract

          Juvenile hormone has been suggested to be a potential mediator in the trade-off between mating and insects’ immunity. Studies on various insect taxons have found that juvenile hormone interferes with humoral and cellular immunity. Although this was shown experimentally, studies using highly virulent parasites or pathogens are lacking so far. In this study, we tested if juvenile hormone administration affected resistance against entomopathogenic fungi, Metarhizium robertsii, in the mealworm beetle, Tenebrio molitor. In previous studies with T. molitor, juvenile hormone has been found to reduce a major humoral immune effector-system (phenoloxidase) in both sexes and decrease the encapsulation response in males. Here, we found that juvenile hormone administration prolonged survival time after infection with M. robertsii in males but reduced survival time in females. This study indicates that the effects of juvenile hormone on insect immunity might be more complicated than previously considered. We also suggest that there might be a trade-off between specific and non-specific immunity since, in males, juvenile hormone enhances specific immunity but corrupts non-specific immunity. Our study highlights the importance of using real parasites and pathogens in immuno-ecological studies.

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          Immune defense and host life history.

          Recent interest has focused on immune response in an evolutionary context, with particular attention to disease resistance as a life-history trait, subject to trade-offs against other traits such as reproductive effort. Immune defense has several characteristics that complicate this approach, however; for example, because of the risk of autoimmunity, optimal immune defense is not necessarily maximum immune defense. Two important types of cost associated with immunity in the context of life history are resource costs, those related to the allocation of essential but limited resources, such as energy or nutrients, and option costs, those paid not in the currency of resources but in functional or structural components of the organism. Resource and option costs are likely to apply to different aspects of resistance. Recent investigations into possible trade-offs between reproductive effort, particularly sexual displays, and immunity have suggested interesting functional links between the two. Although all organisms balance the costs of immune defense against the requirements of reproduction, this balance works out differently for males than it does for females, creating sex differences in immune response that in turn are related to ecological factors such as the mating system. We conclude that immune response is indeed costly and that future work would do well to include invertebrates, which have sometimes been neglected in studies of the ecology of immune defense.
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            Parasites, Bright Males, and the Immunocompetence Handicap

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              Insect hemocytes and their role in immunity.

              The innate immune system of insects is divided into humoral and cellular defense responses. Humoral defenses include antimicrobial peptides, the cascades that regulate coagulation and melanization of hemolymph, and the production of reactive intermediates of oxygen and nitrogen. Cellular defenses refer to hemocyte-mediated responses like phagocytosis and encapsulation. In this review, we discuss the cellular immune responses of insects with emphasis on studies in Lepidoptera and Diptera. Insect hemocytes originate from mesodermally derived stem cells that differentiate into specific lineages identified by morphology, function, and molecular markers. In Lepidoptera, most cellular defense responses involve granular cells and plasmatocytes, whereas in Drosophila they involve primarily plasmatocytes and lamellocytes. Insect hemocytes recognize a variety of foreign targets as well as alterations to self. Both humoral and cell surface receptors are involved in these recognition events. Once a target is recognized as foreign, hemocyte-mediated defense responses are regulated by signaling factors and effector molecules that control cell adhesion and cytotoxicity. Several lines of evidence indicate that humoral and cellular defense responses are well-coordinated with one another. Cross-talk between the immune and nervous system may also play a role in regulating inflammation-like responses in insects during infection.
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                Author and article information

                Journal
                J Fungi (Basel)
                J Fungi (Basel)
                jof
                Journal of Fungi
                MDPI
                2309-608X
                19 November 2020
                December 2020
                : 6
                : 4
                : 298
                Affiliations
                [1 ]Department of Biology, Section of Ecology, University of Turku, FI-20014 Turku, Finland; mjranta@ 123456utu.fi (M.J.R.); mari.polkki@ 123456hotmail.com (M.P.)
                [2 ]Laboratory of Biological Plant Protection and Biotechnology, Department Plant Protection, Novosibirsk State Agrarian University, 630039 Novosibirsk, Russia; dubovskiy2000@ 123456yahoo.com
                [3 ]Siberian Federal Scientific Centre of Agro-BioTechnologies, Russian Academy of Sciences, 630501 Krasnoobsk, Russia
                [4 ]Department of Biotechnology, Daugavpils University, 5401 Daugavpils, Latvia; tatjana.krama@ 123456du.lv
                [5 ]Department of Plant Health, Estonian University of Life Sciences, 51006 Tartu, Estonia
                [6 ]Laboratorio de Ecología Evolutiva, Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico; jcg@ 123456enesmorelia.unam.mx
                [7 ]Institute of Ecology and Earth Sciences, University of Tartu, 51014 Tartu, Estonia
                [8 ]Department of Zoology and Animal Ecology, Faculty of Biology, University of Latvia, 1004 Rīga, Latvia
                Author notes
                [* ]Correspondence: indrikis.krams@ 123456ut.ee ; Tel.: +371-2946-5273
                Author information
                https://orcid.org/0000-0001-9691-3960
                https://orcid.org/0000-0002-9231-0641
                https://orcid.org/0000-0001-7150-4108
                Article
                jof-06-00298
                10.3390/jof6040298
                7711818
                33227937
                2fbd84f3-e790-4997-a636-b1a6fd7230f9
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 17 September 2020
                : 16 November 2020
                Categories
                Article

                immune defense,immunocompetence,metarhizium robertsii,pathogens,sex,tenebrio molitor

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