Climate change facilitates a parasite’s host exploitation via temperature‐mediated immunometabolic processes

Abstract

Global climate change can influence organismic interactions like those between hosts and parasites. Rising temperatures may exacerbate the exploitation of hosts by parasites, especially in ectothermic systems. The metabolic activity of ectotherms is strongly linked to temperature and generally increases when temperatures rise. We hypothesized that temperature change in combination with parasite infection interferes with the host's immunometabolism. We used a parasite, the avian cestode Schistocephalus solidus, which taps most of its resources from the metabolism of an ectothermic intermediate host, the three-spined stickleback. We experimentally exposed sticklebacks to this parasite, and studied liver transcriptomes 50 days after infection at 13°C and 24°C, to assess their immunometabolic responses. Furthermore, we monitored fitness parameters of the parasite and examined immunity and body condition of the sticklebacks at 13°C, 18°C and 24°C after 36, 50 and 64 days of infection. At low temperatures (13°C), S. solidus growth was constrained, presumably also by the more active stickleback's immune system, thus delaying its infectivity for the final host to 64 days. Warmer temperature (18°C and 24°C) enhanced S. solidus growth, and it became infective to the final host already after 36 days. Overall, S. solidus produced many more viable offspring after development at elevated temperatures. In contrast, stickleback hosts had lower body conditions, and their immune system was less active at warm temperature. The stickleback's liver transcriptome revealed that mainly metabolic processes were differentially regulated between temperatures, whereas immune genes were not strongly affected. Temperature effects on gene expression were strongly enhanced in infected sticklebacks, and even in exposed-but-not-infected hosts. These data suggest that the parasite exposure in concert with rising temperature, as to be expected with global climate change, shifted the host's immunometabolism, thus providing nutrients for the enormous growth of the parasite and, at the same time suppressing immune defence.

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition

“…However, we recently observed an impact of exposure on threespine stickleback hepatosomatic index and body condition, traditionally used as a measure of host condition (Chellappa et al, 1995; Piecyk, Ritter, et al, 2019). Likewise, a recent study showed a equally strong impact of exposure and infection on the liver transcriptome, with an increase in expression of genes involved in cellular turnover and metabolic processes (Scharsack et al, 2021). This reduced host condition and shift in metabolic activity upon exposure suggests that the cost of resistance to infection, and elimination of the parasite through cell‐mediated immunity within the first 2 weeks of infection (Kurtz et al, 2004) could indirectly impact the microbiome of exposed sticklebacks.…”

Moderate climate warming scenarios during embryonic and post‐embryonic stages benefit a cold‐climate lizard

“…These extreme climatic conditions can result in direct mortality (Hall & Sun, 2021; Sun et al., 2021), or indirectly depress survival by imposing physiological stress, weakening immunocompetence and resistance to parasites (e.g. Scharsack et al., 2021; Sun, Wang, et al., 2018; Wang et al., 2016; Zhang et al., 2018). Alternatively, the higher survival rate of hatchlings in warming climates might be due to treatment‐induced enhancement in performance (e.g.…”

No strong associations between temperature and the host–parasite interaction in wild stickleback

“…In this study the authors have used a correlational, natural experimental approach to investigate whether temperature is associated with the outcome of infection for both a wild stickleback host and its cestode parasite. Previous laboratory work found that high temperatures benefitted the parasite while being detrimental to the host (Macnab & Barber, 2012; Scharsack et al ., 2021). Nonetheless, in wild, free‐ranging fish, the authors found little evidence that the outcome of the host–parasite interaction was linked with temperature.…”

“…The fact that the authors did not observe an increase in parasite size through time indicates that hosts with large parasites disappearing from the population were balanced by new infections, with smaller parasites, being established at a similar rate. If infections were established substantially before this study began, then the prevalences observed could also be affected by temperatures at the time of initial exposure, which can affect the success of S. solidus establishment (Scharsack et al ., 2021). Moreover, infection outcomes depend on the hosts’ temperature of origin, such that hosts are less tolerant of infection at unfamiliar temperatures (Franke et al ., 2017).…”

“…The three‐spined stickleback Gasterosteus aculeatus (Linnaeus 1758), a small fish common across the temperate Northern Hemisphere, and its cestode parasite Schistocephalus solidus constitute a well‐established laboratory and wild system for host–parasite interactions in which infection reduces host fitness in terms of both survival and reproductive output (Barber, 2013; Barber & Scharsack, 2010; Budria & Candolin, 2015). Natural temperature gradients and anthropogenic environmental change are associated with S. solidus prevalence in the wild (Budria & Candolin, 2015; Karvonen et al ., 2013), and higher temperatures have been shown in the laboratory to be simultaneously beneficial to the parasite and detrimental to the fish (Franke et al ., 2017; Macnab & Barber, 2012; Scharsack et al ., 2021). This previous work also provides clear predictions for the quantitative relationships the authors expect to find between parasitism, temperature and host performance in the wild.…”