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

• Published in: Global change biology 2021-01, Vol.27 (1), p.94-107
• Main Authors: Scharsack, Jörn P., Wieczorek, Bartholomäus, Schmidt‐Drewello, Alexander, Büscher, Janine, Franke, Frederik, Moore, Andrew, Branca, Antoine, Witten, Anika, Stoll, Monika, Bornberg‐Bauer, Erich, Wicke, Susann, Kurtz, Joachim
• Format: Article
• Language: English
• Subjects: Animals; Body condition; Cestode Infections; Climate Change; Exploitation; Exposure; Fish Diseases; Freshwater fishes; Gasterosteus aculeatus; Gene expression; Growth; High temperature; Host-Parasite Interactions; Hosts; Immune system; Immunity; immunometabolism; Infections; Infectivity; Liver; liver transcriptomics; Low temperature; Metabolism; Nutrients; Offspring; parasite; Parasites; Schistocephalus solidus; Smegmamorpha; Solidus; Temperature; Temperature effects
• ISSN: 1354-1013; 1365-2486
• DOI: 10.1111/gcb.15402

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. Climate change effects on parasite are a major concern. Experimental exposure of a host parasite pair to warm and cold conditions, revealed prominent benefits for the growth of the parasite in warm conditions, while the host growth was impaired. The parasite achieves this by manipulation of gene expression profiles in the hosts liver, thus mobilizing nutrient supply from the