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

• Published in: Proceedings of the Royal Society. B, Biological sciences Vol. 287; no. 1930; p. 20201017
• Main Authors: Whiting, James R., Mahmud, Muayad A., Bradley, Janette E., MacColl, Andrew D. C.
• Format: Journal Article
• Language: English
• Published: The Royal Society 08-07-2020
• Subjects: Ecology
• ISSN: 0962-8452; 1471-2954
• DOI: 10.1098/rspb.2020.1017

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.