Dynamics of infection and immunity over 50 years as marine stickleback adapt to freshwater

ABSTRACT When a species colonizes a new environment, it may encounter new parasites to which its immune system is poorly adapted. After an initial spike in infection rates in the naïve founder population, the host may subsequently evolve increased immunity thereby reducing infection rates. Here, we present an example of this eco-evolutionary process, in a population of threespine stickleback ( Gasterosteus aculeatus ) that was founded in Heisholt Quarry, a man-made quarry pond, in 1967. Marine stickleback rarely encounter Schistocephalus solidus tapeworms (which require freshwater to hatch), and so remain highly susceptible to infection. Initially, introduced marine fish were heavily infected by S.solidus . They exhibited low levels of fibrosis, a heritable immune trait which some genotypes activate in response to infection, thereby suppressing tapeworm growth and viability. By the 1990’s, the Heisholt Quarry population exhibited high rates of fibrosis, which partly suppressed S.solidus infection. This increased immune response led to reduced infection rates and the tapeworm was apparently extirpated by 2021. Because fibrosis has a strong genetic basis in other stickleback populations, we infer that the newly founded stickleback-parasite interaction exhibit an eco-evolutionary process of increased immunity that e_ectively reduced infection. The infection and immune dynamics documented here closely match those expected from a simple eco-evo dynamic model presented here. IMPACT SUMMARY Parasite-host relationships are a great framework within which to study the mechanisms driving evolutionary change, both in terms of ecological dynamics, selection pressures, and the phenotypic basis of adaptation to environmental change. One classic example of adaptation is the loss of armor plating as marine stickleback fish colonize freshwater habitats. However, the parasitological and immunological adaptations in new freshwater populations are less clear. When marine fish colonize freshwater they encounter an unfamiliar tapeworm parasite, Schistocephalus solidus , to which they are poorly adapted. Many (but not all) freshwater populations evolve an inducible fibrosis response to S.solidus , a build-up of scar tissue that limits parasite growth and survival. However, we did not know the time frame over which marine fish, invading freshwater, will evolve this immune trait. To resolve this, we tracked the eco-evolutionary dynamics of Schistocephalus solidus tapeworm infection and the fibrosis immune response over 50 years, in an artificial quarry pond populated by susceptible marine fish in 1967. We show that infection rates were initially high, as the marine fish encountered a freshwater parasite to which they were not adapted. Fibrosis rates subsequently increased, reducing the infection rates and by 2021 S.solidus was apparently eliminated. This process matches a simple eco-evolutionary model of an inducible immune response, and provides a clear example of how hosts can adapt to and suppress novel parasites. Although fibrosis is typically viewed as an immune pathology contributing to disease in humans, we show that in stickleback it has a key adaptive value in protection against helminth infection.

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