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

Scharsack PJ, Wieczorek B, Schmidt-Drewello A, Büscher J, Franke F, Moore A, Branca A, Witten A, Stoll M, Bornberg-Bauer E, Wicke S, Kurtz J

Zusammenfassung

Global climate change can influence organismic interactions like those between hostsand parasites. Rising temperatures may exacerbate the exploitation of hosts by parasites, especially in ectothermic systems. The metabolic activity of ectotherms is stronglylinked to temperature and generally increases when temperatures rise. We hypothesized that temperature change in combination with parasite infection interferes withthe host's immunometabolism. We used a parasite, the avian cestode Schistocephalussolidus, which taps most of its resources from the metabolism of an ectothermic intermediate host, the three-spined stickleback. We experimentally exposed sticklebacks tothis 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 sticklebacksat 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. Warmertemperature (18°C and 24°C) enhanced S. solidus growth, and it became infective tothe final host already after 36 days. Overall, S. solidus produced many more viable offspring after development at elevated temperatures. In contrast, stickleback hosts hadlower 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 stronglyaffected. Temperature effects on gene expression were strongly enhanced in infectedsticklebacks, and even in exposed-but-not-infected hosts. These data suggest that theparasite exposure in concert with rising temperature, as to be expected with global climate change, shifted the host's immunometabolism, thus providing nutrients for theenormous growth of the parasite and, at the same time suppressing immune defence.