The influence of immune activation on thermal tolerance along a latitudinal cline

Abstract

Global change is shifting both temperature patterns and the geographic distribution of pathogens, and infection has already been shown to substantially reduce host thermal performance, potentially placing populations at greater risk that previously thought. But what about individuals that are able to successfully clear an infection? Whilst the direct damage a pathogen causes will likely lead to reductions in host's thermal tolerance, the response to infection often shares many underlying pathways with the general stress response, potentially acting as a buffer against subsequent thermal stress. Here, by exposing Drosophila melanogaster to heat‐killed bacterial pathogens, we investigate how activation of a host's immune system can modify any response to both heat and cold temperature stress. In a single focal population, we find that immune activation can improve a host's knockdown times during heat shock, potentially offsetting some of the damage that would subsequently arise as an infection progresses. Conversely, immune activation had a detrimental effect on CTmax and did not influence lower thermal tolerance as measured by chill‐coma recovery time. However, we also find that the influence of immune activation on heat knockdown times is not generalizable across an entire cline of locally adapted populations. Instead, immune activation led to signals of local adaptation to temperature being lost, erasing the previous advantage that populations in warmer regions had when challenged with heat stress. Our results suggest that activation of the immune system may help buffer individuals against the detrimental impact of infection on thermal tolerance; however, any response will be population specific and potentially not easily predicted across larger geographic scales, and dependent on the form of thermal stress faced by a host.

Microbes increase thermal sensitivity in the mosquito Aedes aegypti, with the potential to change disease distributions

“…aegypti infected with the wMel strain of Wolbachia exhibit reduced maternal transmission rates in response to heat spikes that can lead to the production of uninfected offspring [36]. More recently, several studies in Drosophila species have demonstrated that Wolbachia infection can change the host insect's thermal preference [37], of which the directionality varies by bacterial strain [38] More broadly, infection in invertebrates has been shown to substantially increase host or vector susceptibility to thermal stress [39][40][41][42]. A recent study conducted by Hector et al, 2019 showed that Daphnia magna (water flea) infected with the bacterial pathogen Pasteuria ramosa exhibit a reduction in thermal limits up to 2˚C.…”

“…In Drosophila melanogaster, immune activation induced by bacterial challenge was shown to affect the temperature at which physiological failure occurred, reducing the overall thermal tolerance (i.e. critical thermal maximum) of the host [39]. Parallel studies have not been carried out for the major mosquito vectors of human disease-causing viruses.…”

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

“…Previously, using only female hosts, infection by P. ramosa has been shown to result in a substantial reduction in the thermal limits of its host under both static and ramped forms of heat stress (Hector et al, 2019). This reduction in both critical thermal maxima (CT max) and time to immobilization (i.e., knockdown times) was on par with the changes in thermal limits commonly observed across large geographical ranges for Daphnia (Yampolsky et al, 2014) and other species (Calosi et al, 2010;Hector et al, 2020;Janion-Scheepers et al, 2018;Sgrò et al, 2010). When considered in light of recent studies showing evidence of local adaptation across Daphnia host genotypes (Seefeldt & Ebert, 2019;Yampolsky et al, 2014), and evidence that temperature influences many aspects of pathogen fitness and disease dynamics (Auld & Brand, 2017;Shocket et al, 2018;Vale & Little, 2009), the results of Hector et al (2019) add to the growing recognition that exposure to thermal stress may influence the ecology and evolution of both host and pathogen species.…”

“…When considered in light of recent studies showing evidence of local adaptation across Daphnia host genotypes (Seefeldt & Ebert, 2019;Yampolsky et al, 2014), and evidence that temperature influences many aspects of pathogen fitness and disease dynamics (Auld & Brand, 2017;Shocket et al, 2018;Vale & Little, 2009), the results of Hector et al (2019) add to the growing recognition that exposure to thermal stress may influence the ecology and evolution of both host and pathogen species. In all cases, however, only females have been the direct focus of study, as with many other studies of thermal performance (Calosi et al, 2010;Hector et al, 2020;Janion-Scheepers et al, 2018;Sgrò et al, 2010), and the impact of both thermal stress and infection on male performance remains unknown.…”

“…(2019) add to the growing recognition that exposure to thermal stress may influence the ecology and evolution of both host and pathogen species. In all cases, however, only females have been the direct focus of study, as with many other studies of thermal performance (Calosi et al., 2010; Hector et al., 2020; Janion‐Scheepers et al., 2018; Sgrò et al., 2010), and the impact of both thermal stress and infection on male performance remains unknown.…”