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      Independent effects on cellular and humoral immune responses underlie genotype-by-genotype interactions between Drosophila and parasitoids

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          Abstract

          It is common to find abundant genetic variation in host resistance and parasite infectivity within populations, with the outcome of infection frequently depending on genotype-specific interactions. Underlying these effects are complex immune defenses that are under the control of both host and parasite genes. We have found extensive variation in Drosophila melanogaster’s immune response against the parasitoid wasp Leptopilina boulardi. Some aspects of the immune response, such as phenoloxidase activity, are predominantly affected by the host genotype. Some, such as upregulation of the complement-like protein Tep1, are controlled by the parasite genotype. Others, like the differentiation of immune cells called lamellocytes, depend on the specific combination of host and parasite genotypes. These observations illustrate how the outcome of infection depends on independent genetic effects on different aspects of host immunity. As parasite-killing results from the concerted action of different components of the immune response, these observations provide a physiological mechanism to generate phenomena like epistasis and genotype-interactions that underlie models of coevolution.

          Author summary

          In many species individuals differ greatly in how resistant they are to infection. Resistance frequently depends on the combination of host and parasite genomes—a host which is resistant to one parasite genotype may be susceptible to a different genotype. This has important evolutionary consequences, maintaining genetic variation in populations and driving dynamic changes in the frequency of the genetic variants involved. To understand how differences in the immune response give rise to these genetic interactions, we have studied a parasitic wasp that lays its eggs within the larvae of the fruit fly Drosophila melanogaster. We found that some aspects of the immune response are affected by the host genome, some by the parasite genome, and some by the specific combination of host and parasite. However, no single component of the immune response could predict whether a host killed the parasite. Our results demonstrate how a complex interplay between host and parasite genomes controls different aspects of immunity, ultimately determining whether the host can resist infection.

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          Most cited references37

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          Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines

          The Drosophila melanogaster Genetic Reference Panel (DGRP) is a community resource of 205 sequenced inbred lines, derived to improve our understanding of the effects of naturally occurring genetic variation on molecular and organismal phenotypes. We used an integrated genotyping strategy to identify 4,853,802 single nucleotide polymorphisms (SNPs) and 1,296,080 non-SNP variants. Our molecular population genomic analyses show higher deletion than insertion mutation rates and stronger purifying selection on deletions. Weaker selection on insertions than deletions is consistent with our observed distribution of genome size determined by flow cytometry, which is skewed toward larger genomes. Insertion/deletion and single nucleotide polymorphisms are positively correlated with each other and with local recombination, suggesting that their nonrandom distributions are due to hitchhiking and background selection. Our cytogenetic analysis identified 16 polymorphic inversions in the DGRP. Common inverted and standard karyotypes are genetically divergent and account for most of the variation in relatedness among the DGRP lines. Intriguingly, variation in genome size and many quantitative traits are significantly associated with inversions. Approximately 50% of the DGRP lines are infected with Wolbachia , and four lines have germline insertions of Wolbachia sequences, but effects of Wolbachia infection on quantitative traits are rarely significant. The DGRP complements ongoing efforts to functionally annotate the Drosophila genome. Indeed, 15% of all D. melanogaster genes segregate for potentially damaged proteins in the DGRP, and genome-wide analyses of quantitative traits identify novel candidate genes. The DGRP lines, sequence data, genotypes, quality scores, phenotypes, and analysis and visualization tools are publicly available.
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            Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.

            The extent to which an organism is selected to invest in defences against pathogens and parasites depends on the advantages that ensue should infection occur, but also on the costs of maintaining defences in the absence of infection. The presence of heritable variation in resistance suggests that costs exist, but we know very little about the nature or magnitude of these costs in natural populations of animals. A powerful technique for identifying trade-offs between fitness components is the study of correlated responses to artificial selection. We have selected Drosophila melanogaster for improved resistance against an endoparasitoid, Asobara tabida. Endoparasitoids are insects whose larvae develop internally within the body of other insects, eventually killing them, although their hosts can sometimes survive attack by mounting a cellular immune response. We found that reduced larval competitive ability in unparasitized D. melanogaster is a correlated response to artificial selection for improved resistance against A. tabida. The strength of selection for competitive ability and parasitoid resistance is likely to vary temporally and spatially, which may explain the observed heritable variation in resistance.
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              Evolutionary dynamics of plant R-genes.

              Plant R-genes involved in gene-for-gene interactions with pathogens are expected to undergo coevolutionary arms races in which plant specificity and pathogen virulence continually adapt in response to each other. Lending support to this idea, the solvent-exposed amino acid residues of leucine-rich repeats, a region of R-genes involved in recognizing pathogens, often evolve at unusually fast rates. But within-species polymorphism is also common in R-genes, implying that the adaptive substitution process is not simply one of successive selective sweeps. Here we document these features in available data and discuss them in light of the evolutionary dynamics they likely reflect.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, CA USA )
                1553-7366
                1553-7374
                7 October 2019
                October 2019
                : 15
                : 10
                : e1008084
                Affiliations
                [1 ] Department of Genetics, University of Cambridge, Cambridge, United Kingdom
                [2 ] Antalya Bilim University, Faculty of Engineering, Department of Material Science and Nanotechnology Engineering, Dosemealti, Antalya, Turkey
                Institut Pasteur, FRANCE
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: Università degli Studi di Milano, Dipartimento di Bioscienze, Milano, MI

                Author information
                http://orcid.org/0000-0001-9004-1831
                http://orcid.org/0000-0002-4386-3020
                http://orcid.org/0000-0002-0939-9308
                http://orcid.org/0000-0001-7470-8157
                Article
                PPATHOGENS-D-19-01053
                10.1371/journal.ppat.1008084
                6797232
                31589659
                bd748beb-c1f4-4025-bdec-928211730557
                © 2019 Leitão et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 June 2019
                : 16 September 2019
                Page count
                Figures: 3, Tables: 0, Pages: 13
                Funding
                This work was funded by a Natural Environment Research Council grant NE/P00184X/1 to FMJ and ABL. ABL was supported by an EMBO Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Immunology
                Immune Response
                Medicine and Health Sciences
                Immunology
                Immune Response
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Blood Cells
                White Blood Cells
                Hemocytes
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Immune Cells
                White Blood Cells
                Hemocytes
                Biology and Life Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Hemocytes
                Medicine and Health Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Hemocytes
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Biology and Life Sciences
                Immunology
                Immune Suppression
                Medicine and Health Sciences
                Immunology
                Immune Suppression
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Immune Suppression
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Immune Suppression
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-10-17
                Data are available in the Cambridge Data Repository https://doi.org/10.17863/CAM.44113.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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