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 that some genotypes activate in response to infection, thereby suppressing tapeworm growth and viability. By the 1990s, 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 exhibits an eco-evolutionary process of increased immunity that effectively reduced infection. The infection and immune dynamics documented here closely match those expected from a simple eco-evo dynamic model presented here.