Abstract
Seasonal patterns in immunity are frequently observed in vertebrates but are poorly understood. Here, we focused on a natural piscine model, the three-spined stickleback (Gasterosteus aculeatus), and asked how seasonal immune allocation is driven by physical variables (time, light, and heat). Using functionally-relevant gene expression metrics as a reporter of seasonal immune allocation, we synchronously sampled fish monthly from the wild (two habitats), and from semi-natural outdoors mesocosms (stocked from one of the wild habitats). This was repeated across two annual cycles, with continuous within-habitat monitoring of environmental temperature and implementing a manipulation of temperature in the mesocosms. We also conducted a long-term laboratory experiment, subjecting acclimated wild fish to natural and accelerated (×2) photoperiodic change at 7 and 15°C. The laboratory experiment demonstrated that immune allocation was independent of photoperiod and only a very modest effect, at most, was controlled by a tentative endogenous circannual rhythm. On the other hand, experimentally-determined thermal effects were able to quantitatively predict much of the summer–winter fluctuation observed in the field and mesocosms. Importantly, however, temperature was insufficient to fully predict, and occasionally was a poor predictor of, natural patterns. Thermal effects can thus be overridden by other (unidentified) natural environmental variation and do not take the form of an unavoidable constraint due to cold-blooded physiology. This is consistent with a context-dependent strategic control of immunity in response to temperature variation, and points to the existence of temperature-sensitive regulatory circuits that might be conserved in other vertebrates.
Highlights
Disease risk, in humans and animals, is frequently seasonal and seasonal variation in host immune allocation [1,2,3,4] may contribute to this
Gill tissue was used in this experiment as we have recently shown it to be especially sensitive to seasonal change and to show similar seasonal responses to whole-fish samples [22]
Using a combination of field, mesocosm, and laboratory experi mental observations, we have demonstrated that photoperiodic control of seasonal immune allocation in sticklebacks is negligible
Summary
In humans and animals, is frequently seasonal and seasonal variation in host immune allocation [1,2,3,4] may contribute to this. Seasonal change in immune responses is often reported in vertebrates [5,6,7,8,9] and might constrain not just infectious disease, through effects on immuncompetence, and autoimmune disease, through altering the tendency for immune autoreactivity Despite this importance, the proximal controllers of seasonal variation in immunity. We set out to bridge the gap between the animal house and the field— drawing together elements that embody the experimental control of the former, allowing strong causal inference, and the natural context of the latter We achieved this by combining detailed monitoring of natural populations, experimental manipulations in outdoor semi-natural mesocosms and a long-term laboratory experiment using acclimatized wild animals exposed to gradual (naturalistic), rather than drastic (unnatural), seasonal photo periodic change. In taking such an approach to photoperiodic manipulation, we reduced the possibility that very unnatural photoperiod (PP) changes might confound outcomes through the stress effects of disruption of the circadian machinery [14] or through the formation of aberrant (e.g., unnaturally prolonged) breeding phenotypes [15]
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