Seasonal immunoregulation in a naturally occurring
vertebrate

Brown, M; Hablutzel, P; Friberg, IM; Thomason, AG; Stewart, A; Pachebat, JA; Jackson, JA

Abstract

Background: Fishes show seasonal patterns of immunity, but such phenomena are imperfectly understood in
vertebrates generally, even in humans and mice. As these seasonal patterns may link to infectious disease risk
and individual condition, the nature of their control has real practical implications. Here we characterize seasonal
dynamics in the expression of conserved vertebrate immunity genes in a naturally-occurring piscine model, the
three-spined stickleback.
Results: We made genome-wide measurements (RNAseq) of whole-fish mRNA pools (n = 36) at the end of summer
and winter in contrasting habitats (riverine and lacustrine) and focussed on common trends to filter habitat-specific
from overarching temporal responses. We corroborated this analysis with targeted year-round whole-fish gene
expression (Q-PCR) studies in a different year (n = 478). We also considered seasonal tissue-specific expression (6
tissues) (n = 15) at a third contrasting (euryhaline) locality by Q-PCR, further validating the generality of the patterns
seen in whole fish analyses. Extremes of season were the dominant predictor of immune expression (compared to
sex, ontogeny or habitat). Signatures of adaptive immunity were elevated in late summer. In contrast, late winter
was accompanied by signatures of innate immunity (including IL-1 signalling and non-classical complement
activity) and modulated toll-like receptor signalling. Negative regulators of T-cell activity were prominent amongst
winter-biased genes, suggesting that adaptive immunity is actively down-regulated during winter rather than
passively tracking ambient temperature. Network analyses identified a small set of immune genes that might lie
close to a regulatory axis. These genes acted as hubs linking summer-biased adaptive pathways, winter-biased
innate pathways and other organismal processes, including growth, metabolic dynamics and responses to stress
and temperature. Seasonal change was most pronounced in the gill, which contains a considerable concentration
of T-cell activity in the stickleback.
Conclusions: Our results suggest major and predictable seasonal re-adjustments of immunity. Further consideration
should be given to the effects of such responses in seasonally-occurring disease.

Citation

vertebrate. BMC Genomics, 17(369), https://doi.org/10.1186/s12864-016-2701-7

• Journal Article Type: Article
• Acceptance Date: May 6, 2016
• Online Publication Date: May 18, 2016
• Publication Date: May 18, 2016
• Deposit Date: May 20, 2016
• Publicly Available Date: May 20, 2016
• Journal: BMC Genomics
• Electronic ISSN: 1471-2164
• Publisher: Springer Verlag
• Volume: 17
• Issue: 369
• DOI: https://doi.org/10.1186/s12864-016-2701-7
• Publisher URL: http://dx.doi.org/10.1186/s12864-016-2701-7
• Related Public URLs: http://bmcgenomics.biomedcentral.com/
• Additional Information: Projects : Thermal variation and immunity in ectothermic vertebrates; Grant Number: RPG-301; Grant Number: NE/L013517/1