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Prior exposure to long-day photoperiods alters immune responses and increases susceptibility to parasitic infection in stickleback

Whiting, James R.; Mahmud, Muayad A.; Bradley, Janette E.; MacColl, Andrew D.C.

Authors

James R. Whiting

Muayad A. Mahmud

JAN BRADLEY jan.bradley@nottingham.ac.uk
Professor of Parasitology

ANDREW MACCOLL ANDREW.MACCOLL@NOTTINGHAM.AC.UK
Professor of Evolutionary Ecology



Abstract

Seasonal disease and parasitic infection are common across organisms, including humans, and there is increasing evidence for intrinsic seasonal variation in immune systems. Changes are orchestrated through organisms' physiological clocks using cues such as day length. Ample research in diverse taxa has demonstrated multiple immune responses are modulated by photoperiod, but to date, there have been few experimental demonstrations that photoperiod cues alter susceptibility to infection. We investigated the interactions among photoperiod history, immunity and susceptibility in laboratory-bred three-spined stickleback (a long-day breeding fish) and its external, directly reproducing monogenean parasite Gyrodactylus gasterostei. We demonstrate that previous exposure to long-day photoperiods (PLD) increases susceptibility to infection relative to previous exposure to short days (PSD), and modifies the response to infection for the mucin gene muc2 and Treg cytokine foxp3a in skin tissues in an intermediate 12 L : 12 D photoperiod experimental trial. Expression of skin muc2 is reduced in PLD fish, and negatively associated with parasite abundance. We also observe inflammatory gene expression variation associated with natural inter-population variation in resistance, but find that photoperiod modulation of susceptibility is consistent across host populations. Thus, photoperiod modulation of the response to infection is important for host susceptibility, highlighting new mechanisms affecting seasonality of host-parasite interactions.

Journal Article Type Article
Publication Date Jul 8, 2020
Journal Proceedings of the Royal Society B: Biological Sciences
Print ISSN 1471-2954
Electronic ISSN 1471-2954
Publisher Royal Society, The
Peer Reviewed Peer Reviewed
Volume 287
Issue 1930
APA6 Citation Whiting, J. R., Mahmud, M. A., Bradley, J. E., & MacColl, A. D. (2020). Prior exposure to long-day photoperiods alters immune responses and increases susceptibility to parasitic infection in stickleback. Proceedings of the Royal Society B: Biological Sciences, 287(1930), https://doi.org/10.1098/rspb.2020.1017
DOI https://doi.org/10.1098/rspb.2020.1017
Keywords General Biochemistry, Genetics and Molecular Biology; General Immunology and Microbiology; General Agricultural and Biological Sciences; General Environmental Science; General Medicine
Publisher URL https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1017
Additional Information Received: 2020-05-04; Accepted: 2020-06-08; Published: 2020-07-01

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