Lag of Immunity Across Seasonal Acclimation States in Gopher Tortoises (Gopherus Polyphemus)

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Abstract

Disease outbreaks are of increasing importance to ectothermic vertebrates as one of numerous results of global change. Anthropogenic climate change is predicted to increase climatic instability, thereby altering natural thermal environments. In this study, we evaluated the direct effects of rapid temperature change on immunity in Gopher Tortoises (Gopherus polyphemus). Specifically, we tested the lag hypothesis, which predicts significant misalignment of optimal and realized immunity when temperature rapidly changes. We assayed constitutive innate immunity, B-cell humoral responses, and heterophil: lymphocyte ratios in response to rapid temperature changes corresponding to realistic changes in body temperature between winter and summer. We found that during summer, rapid temperature reduction caused a series of changes in immunity, including reduced bactericidal ability (P = 0.002), reduced humoral response (P < 0.0001), and increased heterophil:lymphocyte ratios (P < 0.0001). During winter, we found that a temperature increase provided no benefit to immunity. Specifically, there was no increase in bactericidal ability as was predicted by the lag hypothesis. In winter, humoral responses were significantly reduced as a result of rapid warming (P = 0.011) and the rapid warming caused a significant reduction in heterophil:lymphocyte ratios (P < 0.0001). Independent of temperature, we found a significant acclimation effect of winter relative to summer conditions in humoral response (P < 0.001), which showed an overall increase in this parameter during winter. Our findings demonstrate that rapid temperature change, regardless of its direction, is a constraint on immunity in ectothermic vertebrates.

GRAPHICAL ABSTRACT

We examined the role that rapid temperature change has on Gopherus polyphemus immunity and found that rapid temperature reductions during summer significantly negatively affect immunity. However, rapid temperature increases during winter provide no measurable immunological benefit.

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