In dynamic systems, organisms are faced with variable selective forces that may impose trade-offs. In estuaries, salinity is a strong driver of organismal diversity, while parasites shape species distributions and demography. We tested for trade-offs between low-salinity stress and parasitism in an invasive castrating parasite and its mud crab host along salinity gradients of two North Carolina rivers. We performed field surveys every six to eight weeks over 3 years to determine factors influencing parasite prevalence, host abundance, and associated taxa diversity. We also looked for signatures of low-salinity stress in the host by examining its response (time-to-right and gene expression) to salinity. We found salinity and temperature significantly affected parasite prevalence, with low-salinity sites (less than 10 practical salinity units (PSU)) lacking infection, and populations in moderate salinities at warmer temperatures reaching prevalence as high as 60%. Host abundance was negatively associated with parasite prevalence. Host gene expression was plastic to acclimation salinity, but several osmoregulatory and immune-related genes demonstrated source-dependent salinity response. We identified a genetic marker that was strongly associated with salinity against a backdrop of no neutral genetic structure, suggesting possible selection on standing variation. Our study illuminates how selective trade-offs in naturally dynamic systems may shape host evolutionary ecology.
