Half the story : thermal effects on within-host infectious disease progression in a warming climate

Stewart, A; Hablutzel, PI; Brown, M; Watson, HV; Parker-Norman, S; Tober, AV; Thomason, AG; Friberg, IM; Cable, J; Jackson, JA

Abstract

Immune defence is temperature-dependent in cold-blooded vertebrates (CBVs) and thus directly impacted by global warming. We asked whether immunity and within-host infectious disease progression are altered in CBVs under realistic climate warming in a seasonal mid-latitude setting. Going further, we also asked how large thermal effects are in relation to the effects of other environmental variation in such a setting (critical to our ability to project infectious disease dynamics from thermal relationships alone). We employed the three-spined stickleback and three ecologically-relevant parasite infections as a “wild” model. To generate a realistic climatic warming scenario we used naturalistic outdoors mesocosms with precise temperature control. We also conducted laboratory experiments to estimate thermal effects on immunity and within-host infectious disease progression under controlled conditions. As experimental readouts we measured disease progression for the parasites and expression in 14 immune-associated genes (providing insight into immunophenotypic responses). Our mesocosm experiment demonstrated significant perturbation due to modest warming (+2°C), altering the magnitude and phenology of disease. Our laboratory experiments demonstrated substantial thermal effects. Prevailing thermal effects were more important than lagged thermal effects and disease progression increased or decreased in severity with increasing temperature in an infection-specific way. Combining laboratory-determined thermal effects with our mesocosm data, we used inverse modelling to partition seasonal variation in Saprolegnia disease progression into a thermal effect and a latent immunocompetence effect (driven by non-thermal environmental variation and correlating with immune gene expression). The immunocompetence effect was large, accounting for at least as much variation in Saprolegnia disease as the thermal effect. This suggests that managers of CBV populations in variable environments may not be able to reliably project infectious disease risk from thermal data alone. Nevertheless, such projections would be improved by primarily considering prevailing (not lagged) temperature variation and by incorporating validated measures of individual immunocompetence.

Citation

Stewart, A., Hablutzel, P., Brown, M., Watson, H., Parker-Norman, S., Tober, A., …Jackson, J. (2018). Half the story : thermal effects on within-host infectious disease progression in a warming climate. Global Change Biology, 24(1), 371-386. https://doi.org/10.1111/gcb.13842

• Journal Article Type: Article
• Acceptance Date: Jul 12, 2017
• Online Publication Date: Jul 26, 2017
• Publication Date: Jan 1, 2018
• Deposit Date: Jul 13, 2017
• Publicly Available Date: Jul 26, 2018
• Journal: Global Change Biology
• Print ISSN: 1354-1013
• Electronic ISSN: 1365-2486
• Publisher: Wiley
• Volume: 24
• Issue: 1
• Pages: 371-386
• DOI: https://doi.org/10.1111/gcb.13842
• Publisher URL: http://dx.doi.org/10.1111/gcb.13842
• Related Public URLs: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2486
• Additional Information: Projects : Thermal variation and immunity in ectothermic vertebrates