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    Mating precedes selective immune priming which is maintained throughout bumblebee queen diapause


    Colgan, Thomas J. and Finlay, Sive and Brown, Mark J.F. and Carolan, James C. (2019) Mating precedes selective immune priming which is maintained throughout bumblebee queen diapause. BMC Genomics, 20 (959). ISSN 1471-2164

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    Abstract

    Background: Understanding the mechanisms by which organisms adapt to unfavourable conditions is a fundamental question in ecology and evolutionary biology. One such mechanism is diapause, a period of dormancy typically found in nematodes, fish, crustaceans and insects. This state is a key life-history event characterised by arrested development, suppressed metabolism and increased stress tolerance and allows an organism to avoid prolonged periods of harsh and inhospitable environmental conditions. For some species, diapause is preceded by mating which can have a profound effect on female behaviour, physiology and key biological processes, including immunity. However, our understanding of how mating impacts long-term immunity and whether these effects persist throughout diapause is currently limited. To address this, we explored molecular changes in the haemolymph of the ecologically important pollinator, the buff-tailed bumblebee Bombus terrestris. B. terrestris queens mate prior to entering diapause, a non-feeding period of arrested development that can last 6–9 months. Using mass-spectrometry-based proteomics, we quantified changes in the pre-diapause queen haemolymph after mating, as well as the subsequent protein expression of mated queens during and post-diapause. Results: Our analysis identified distinct proteome profiles associated with diapause preparation, maintenance and termination. More specifically, mating pre-diapause was followed by an increase in the abundance of antimicrobial peptides, key effectors of the immune system. Furthermore, we identified the elevated abundance of these proteins to be maintained throughout diapause. This finding was in contrast to the general reduction observed in immune proteins during diapause suggestive of selective immune priming and expression during diapause. Diapause also affected the expression of proteins involved in cuticular maintenance, olfaction, as well as proteins of unknown function, which may have roles in diapause regulation. Conclusions: Our results provide clear molecular evidence for the consequences and benefits of mating at the immune level as it precedes the selective increased abundance of antimicrobial peptides that are sustained throughout diapause. In addition, our results provide novel insights into the molecular mechanisms by which bumblebees prepare for, survive, and recover from diapause, insights that may have implications for our general understanding of these processes in other insect groups.

    Item Type: Article
    Additional Information: © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Colgan, T.J., Finlay, S., Brown, M.J.F. et al. Mating precedes selective immune priming which is maintained throughout bumblebee queen diapause. BMC Genomics 20, 959 (2019). https://doi.org/10.1186/s12864-019-6314-9 Funding: This publication has emanated from research conducted with the financial support of Science Foundation Ireland (http://www.sfi.ie/) grant EEEOBF131 to MJFB. This funding was used to support sample collection and massspectrometry analysis of haemolymph samples.
    Keywords: Diapause; Immunity; Mating; Mass spectrometry-based proteomics; Bumblebees; Pollinator health;
    Academic Unit: Faculty of Science and Engineering > Biology
    Item ID: 13517
    Identification Number: https://doi.org/10.21203/rs.2.15453/v3
    Depositing User: James Carolan
    Date Deposited: 10 Nov 2020 15:02
    Journal or Publication Title: BMC Genomics
    Publisher: Biomed Central
    Refereed: Yes
    Funders: Science Foundation Ireland (SFI)
    URI:

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