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Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution

Heredityvolume 121pages225238 (2018) | Download Citation

Abstract

Parental experience with parasites and pathogens can lead to increased offspring resistance to infection, through a process known as transgenerational immune priming (TGIP). Broadly defined, TGIP occurs across a wide range of taxa, and can be viewed as a type of phenotypic plasticity, with hosts responding to the pressures of relevant local infection risk by altering their offspring’s immune defenses. There are ever increasing examples of both invertebrate and vertebrate TGIP, which go beyond classical examples of maternal antibody transfer. Here we critically summarize the current evidence for TGIP in both invertebrates and vertebrates. Mechanisms underlying TGIP remain elusive in many systems, but while it is unlikely that they are conserved across the range of organisms with TGIP, recent insight into epigenetic modulation may challenge this view. We place TGIP into a framework of evolutionary ecology, discussing costs and relevant environmental variation. We highlight how the ecology of species or populations should affect if, where, when, and how TGIP is realized. We propose that the field can progress by incorporating evolutionary ecology focused designs to the study of the so far well chronicled, but mostly descriptive TGIP, and how rapidly developing -omic methods can be employed to further understand TGIP across taxa.

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Acknowledgements

We thank Paul Schmid-Hempel for his guidance in the field of Ecological Immunology with more than a decade of inspiring discussions, and for creating an academic environment that fostered the intellectual and personal relationships that produced this manuscript and many others. We also thank the editors of this special issue, Becky Rosengaus, and two anonymous reviewers for constructive comments on the manuscript. OR was supported by Research Grants from the Volkswagen Stiftung, the German Research Foundation (DFG: 237263721; 349393951; 274695381) and a Starting Grant from the European Research Council (MALEPREG). AB was supported by a stipend from the International Max Planck Research School for Evolutionary Biology (IMPRS). SMB was supported by the kindness and naiveté of strangers. BMS was supported by National Science Foundation IOS 16-54028 and an Illinois State University New Faculty Research Initiative Grant.

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  1. Marine Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbrookerweg 20, 24105, Kiel, Germany

    • Olivia Roth
    •  & Anne Beemelmanns
  2. Department of Ocean Sciences, Memorial University of Newfoundland, 0 Marine Lab Rd, St. John’s, NL, Canada

    • Anne Beemelmanns
  3. Institute of Integrative Biology, University of Liverpool, Crown Street, Liverpool, L69 7ZB, UK

    • Seth M. Barribeau
  4. School of Biological Sciences, Illinois State University, Normal, IL, 61790-4120, USA

    • Ben M. Sadd

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The authors declare that they have no conflict of interest.

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Correspondence to Olivia Roth.

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https://doi.org/10.1038/s41437-018-0101-2

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