Resist Globally, Infect Locally: A Transcontinental Test of Adaptation by Stickleback and Their Tapeworm Parasite

Abstract

Parasite infections are a product of both ecological processes affecting host-parasite encounter rates and evolutionary dynamics affecting host susceptibility. However, few studies examine natural infection variation from both ecological and evolutionary perspectives. Here, we describe the ecological and evolutionary factors generating variation in infection rates by a tapeworm (Schistocephalus solidus) in a vertebrate host, the threespine stickleback (Gasterosteus aculeatus). To explore ecological aspects of infection, we measured tapeworm prevalence in Canadian stickleback inhabiting two distinct environments: marine and freshwater. Consistent with ecological control of infection, the tapeworm is very rare in marine environments, even though marine fish are highly susceptible. Conversely, commonly infected freshwater stickleback exhibit substantial resistance in controlled laboratory trials, suggesting that high exposure risk overwhelms their recently evolved resistance. We also tested for parasite adaptation to its host by performing transcontinental reciprocal infections, using stickleback and tapeworm populations from Europe and western Canada. More infections occurred in same-continent host-parasite combinations, indicating parasite "local" adaptation, at least on the scale of continents. However, the recently evolved immunity of freshwater hosts applies to both local and foreign parasites. The pattern of adaptation described here is not wholly compatible with either of the common models of host-parasite coevolution (i.e., matching infection or targeted recognition). Instead, we propose a hybrid, eco-evolutionary model to explain the remarkable pattern of global host resistance and local parasite infectivity.

Consequences of divergent temperature optima in a host–parasite system

“…Stickleback populations vary in resistance to S. solidus, some resistant populations defend themselves from the parasite more often (Kalbe et al 2016, Weber et al 2017a) and if infected, constrain parasite growth more efficiently than sticklebacks from susceptible populations (Kalbe et al 2016, Hamley et al 2017, Weber et al 2017b. It was suggested that acquired immune activity constrains S. solidus growth (Kurtz et al 2004), but innate immune traits, such as frequencies and respiratory burst activity of granulocytes, was correlated to variation in S. solidus resistance across stickleback populations (Hamley et al 2017, Weber et al 2017b).…”

Early stages of infection of three‐spined stickleback (Gasterosteus aculeatus) with the cestode Schistocephalus solidus

“…() were from Germany (Neustädter Binnenwasser). It has been observed that S. solidus prevalence varies across different stickleback populations, which seems to trigger local adaptations of host resistance and parasite virulence (Franke, Armitage, Kutzer, Kurtz, & Scharsack, ; Hamley, Franke, Kurtz, & Scharsack, ; Kalbe, Eizaguirre, Scharsack, & Jakobsen, ; Prieto et al., ; Weber et al., ). Thus, local adaptation might explain the differences in parasite infection and immune kinetics between the present study and the study by Scharsack et al.…”

“…Though, in the present study, sticklebacks and S. solidus originated from Spain (Xinzo de Limia), whereas the fish and parasites used by Scharsack et al (2007) were from Germany (Neustädter Binnenwasser). It has been observed that S. solidus prevalence varies across different stickleback populations, which seems to trigger local adaptations of host resistance and parasite virulence (Franke, Armitage, Kutzer, Kurtz, & Scharsack, 2017;Hamley, Franke, Kurtz, & Scharsack, 2017;Kalbe, Eizaguirre, Scharsack, & Jakobsen, 2016;Prieto et al, 2005;Weber et al, 2017).…”

A eDNA-qPCR assay to non-invasively detect the presence of the parasiteSchistocephalus solidusinside its threespine stickleback host

“…Studying these parasite-hosts interactions requires to be The whole life cycle of this parasite can be reproduced in the laboratory (Barber and 56 Scharsack 2010), which makes it highly amenable to manipulation. However, the 57 success rate of infection in the laboratory when experimental single infections are used 58 is around 15-20% ( (Grécias et al 2016); (Weber et al 2017)). Thus, a high number of 59 individuals must be included and assayed in a study to obtain an acceptable final 60 sample size of infected ones.…”

“…Thus, a high number of 59 individuals must be included and assayed in a study to obtain an acceptable final 60 sample size of infected ones. Furthermore, variation in infection rates for sticklebacks 61 caught in the wild is high (Weber et al 2017), which means that wild individuals 62 considered as uninfected controls may turn out to be infected when studying wild 63 sticklebacks. A simple detection method would allow selecting, or avoiding, infected 64 individuals depending on the needs of a specific project.…”