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      Genetic slippage after sex maintains diversity for parasite resistance in a natural host population

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Although parasite-mediated selection is a major driver of host evolution, its influence on genetic variation for parasite resistance is not yet well understood. We monitored resistance in a large population of the planktonic crustacean Daphnia magna over 8 years, as it underwent yearly epidemics of the bacterial pathogen Pasteuria ramosa. We observed cyclic dynamics of resistance: Resistance increased throughout the epidemics, but susceptibility was restored each spring when hosts hatched from sexual resting stages. Host resting stages collected across the year showed that largely resistant host populations can produce susceptible sexual offspring. A genetic model of resistance developed for this host-parasite system, based on multiple loci and strong epistasis, is in partial agreement with our findings. Our results reveal that, despite strong selection for resistance in a natural host population, genetic slippage after sexual reproduction can be a strong factor for the maintenance of genetic diversity of host resistance.

          Abstract

          Abstract

          Long-term monitoring of a planktonic crustacean’s natural population reveals a cyclic pattern of pathogen resistance.

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          Host-parasite 'Red Queen' dynamics archived in pond sediment.

          Ellen Decaestecker, Sabrina Gaba, Joost A M Raeymaekers … (2007)
          Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.
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            The evolutionary enigma of sex.

            Sarah P. Otto (2009)
            Sexual reproduction entails a number of costs, and yet the majority of eukaryotes engage in sex, at least occasionally. In this article, I review early models to explain the evolution of sex and why they failed to do so. More recent efforts have attempted to account for the complexities of evolution in the real world, with selection that varies over time and space, with differences among individuals in the tendency to reproduce sexually, and with populations that are limited in size. These recent efforts have clarified the conditions that are most likely to explain why sex is so common, as exemplified by the articles in this symposium issue of the American Naturalist.
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              Experimental evolution of parasites.

              Antje D. Ebert (1998)
              Serial passage experiments are a form of experimental evolution that is frequently used in applied sciences; for example, in vaccine development. During these experiments, molecular and phenotypic evolution can be monitored in real time, providing insights into the causes and consequences of parasite evolution. Within-host competition generally drives an increase in a parasite's virulence in a new host, whereas the parasite becomes avirulent to its former host, indicating a trade-off between parasite fitnesses on different hosts. Understanding why parasite virulence seldom escalates similarly in natural populations could help us to manage virulence and deal with emerging diseases.
              Article 0 comments Cited 142 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Camille Ameline:
                ORCID: https://orcid.org/0000-0001-6892-2819
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing
                Felix Voegtli: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing
                Jason Andras:
                ORCID: https://orcid.org/0000-0001-5042-6833
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Validation
                Eric Dexter:
                ORCID: https://orcid.org/0000-0003-2296-9923
                Role: Formal analysisRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing - review & editing
                Jan Engelstädter:
                ORCID: https://orcid.org/0000-0003-3340-918X
                Role: SoftwareRole: Writing - review & editing
                Dieter Ebert: Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing - review & editing
                Journal
                Journal ID (nlm-ta): Sci Adv
                Journal ID (iso-abbrev): Sci Adv
                Journal ID (publisher-id): sciadv
                Journal ID (hwp): advances
                Title: Science Advances
                Publisher: American Association for the Advancement of Science
                ISSN (Electronic): 2375-2548
                Publication date Collection: November 2022
                Publication date (Electronic, pub): 18 November 2022
                Volume: 8
                Issue: 46
                Electronic Location Identifier: eabn0051
                Affiliations
                [ 1 ]Department of Environmental Sciences, Zoology, University of Basel, Vesalgasse 1, 4051 Basel, Switzerland.
                [ 2 ]School of Biological Sciences, The University of Queensland, Brisbane, Australia.
                Author notes
                [* ]Corresponding author. Email: cameline8@ 123456gmail.com
                [†]

                Present address: Evolutionary Biology, Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal.

                [‡]

                Present address: Department of Biological Sciences, Clapp Laboratory, Mount Holyoke College, South Hadley, MA, USA.

                Author information
                https://orcid.org/0000-0001-6892-2819
                https://orcid.org/0000-0001-5042-6833
                https://orcid.org/0000-0003-2296-9923
                https://orcid.org/0000-0003-3340-918X
                Article
                Publisher ID: abn0051
                DOI: 10.1126/sciadv.abn0051
                PMC ID: 9674289
                PubMed ID: 36399570
                SO-VID: b3afb657-c075-4cdd-b7c2-5bba6365f7a9
                Copyright © Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                Date received : 01 November 2021
                Date accepted : 04 October 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100008375, Universität Basel;
                Funded by: FundRef http://dx.doi.org/10.13039/100009736, Freiwillige Akademische Gesellschaft;
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 310030B_166677
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 310030_188887
                Categories
                Subject: Research Article
                Subject: Biomedicine and Life Sciences
                Subject: SciAdv r-articles
                Subject: Evolutionary Biology
                Subject: Genetics
                Subject: Evolutionary Biology
                Custom metadata
                Copyeditor Nicole Falcasantos

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