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Trans-generational viral transmission and immune priming are dose-dependent

Trans-generational viral transmission and immune priming are dose-dependent

Wilson, Kenneth ORCID logoORCID: https://orcid.org/0000-0001-5264-6522, Grzywacz, David, Cory, Jenny S., Donkersley, Philip ORCID logoORCID: https://orcid.org/0000-0001-6013-1043 and Graham, Robert I. (2021) Trans-generational viral transmission and immune priming are dose-dependent. The Journal of Animal Ecology, 90 (6). pp. 1560-1569. ISSN 0021-8790 (Print), 1365-2656 (Online) (doi:10.1111/1365-2656.13476)

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Abstract

It is becoming increasingly apparent that trans-generational immune priming (i.e. the transfer of the parental immunological experience to its progeny resulting in offspring protection from pathogens that persist across generations) is a common phenomenon not only in vertebrates, but also invertebrates. Likewise, it is known that covert pathogenic infections may become 'triggered' into an overt infection by various stimuli, including exposure to heterologous infections. Yet rarely have both phenomena been explored in parallel. Using as a model system the African armyworm (Spodoptera exempta), an eruptive agricultural pest, and its endemic dsDNA virus (Spodoptera exempta nucleopolyhedrovirus, SpexNPV), the aim of this study was to explore the impact of parental inoculating-dose on trans-generational pathogen transmission and immune priming (in its broadest sense). Larvae were orally-challenged with one of five doses of SpexNPV and survivors from these treatments were mated and their offspring monitored for viral mortality. Offspring from parents challenged with low viral doses showed evidence of 'immune priming' (i.e. enhanced survival following SpexNPV challenge); in contrast, offspring from parents challenged with higher viral doses exhibited greater susceptibility to viral challenge. Most offspring larvae died of the virus they were orally-challenged with; in contrast, most offspring from parents that had been challenged with the highest doses were killed by the vertically-transmitted virus (90%) and not the challenge virus. These results demonstrate that the outcome of a potentially lethal virus challenge is critically dependent on the level of exposure to virus in the parental generation - either increasing resistance at very low parental viral doses (consistent with trans-generational immune-priming) or increasing susceptibility at higher parental doses (consistent with virus triggering). We discuss the implications of these findings for understanding both natural epizootics of baculoviruses and for using them as biological control agents.

Item Type: Article
Additional Information: © 2021 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 Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Uncontrolled Keywords: baculovirus, immune-priming, outbreak pest, vertical transmission, virus triggering
Subjects: S Agriculture > S Agriculture (General)
Faculty / School / Research Centre / Research Group: Faculty of Engineering & Science
Faculty of Engineering & Science > Natural Resources Institute
Faculty of Engineering & Science > Natural Resources Institute > Centre for Sustainable Agriculture 4 One Health
Faculty of Engineering & Science > Natural Resources Institute > Centre for Sustainable Agriculture 4 One Health > Behavioural Ecology
SWORD Depositor: Users 6393 not found.
Last Modified: 27 Nov 2024 14:29
URI: http://gala.gre.ac.uk/id/eprint/31963

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