Local adaptation of immunity against a trematode parasite in marine amphipod populations

Abstract

Resources allocated to defence against parasites are not available for investment in other functions such as growth or reproduction, resulting in trade-offs between different components of an organism’s fitness. In balancing the cost of infection and the cost of immunity, selection should only favour individuals that allocate more energy to resistance and immune responses in populations regularly exposed to debilitating parasites. Here, we compare the ability of amphipods, Paracalliope novizealandiae, to (1) avoid becoming infected and (2) to respond to infection by encapsulating and melanizing parasites, between two natural populations exposed to different risk of parasitism. One population faces high levels of infection by the debilitating trematode parasite Maritrema novaezealandensis, whereas the other population is not parasitised by this trematode nor by any other parasite. Under controlled experimental conditions, with exposure to a standardized dose of parasites, amphipods from the parasite-free population acquired significantly more parasites than those from the population regularly experiencing infection. Furthermore, a lower frequency of amphipods from the parasite-free population succeeded at melanizing (and thus killing) parasites, and they melanized a lower percentage of parasites on average, than amphipods from the parasitised population. These differences persist when individual factors, such as amphipod sex or body length, are taken into account as potential confounding variables. These results support the existence of local adaptation against parasites: an amphipod population that never experiences trematode infections is less capable of resisting infection, both in terms of its first line of defence (avoiding infection) and a later line of defence (fighting parasites following infection), than a population regularly exposed to infection.