Physical cues controlling seasonal immune allocation in a natural piscine model

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 functional 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 withinhabitat 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, experimental 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