Loma morhua infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential effects on host growth among family lines

Microsporidia are emerging as a threat to productivity of commercial finfish aquaculture because of high-prevalence infections facilitated by direct transmission. Infection dynamics are poorly understood for most microsporidians and inability to reliably quantify differential infections impedes disease mitigation strategies that could select broodstock with inherent disease-resistant phenotypes. Moreover, investigations of suitable biomarkers that link immune function with disease susceptibility of fishes are limited. Herein, we observe an inverse relationship between fish growth and infection status with the microsporidium Loma morhua among 50 different Atlantic cod (Gadus morhua) family lines. We present a standardized template for quantifying parasite infection intensity, with the spleen being the most reliable organ for comparing natural infections and for monitoring experimental infections. Variability in infection intensities among 50 cod families suggests that differential susceptibility to L. morhua has a genetic basis. Ultra-deep Illumina sequencing identified 299 major histocompatibility class I (MH-I) variants from this regionally restricted 50-family cod population. Variation in Atlantic cod susceptibility might reflect hyper-diversification of MH-I genes and individual variability in the ability to present endogenous pathogen antigens during cell-mediated immune responses. Relevance of MH-I expansion to selective breeding for disease resistance remains poorly characterized. Importantly, differential susceptibility to L. morhua revealed impaired fish growth, resulting in a 14% reduction in fillet mass in susceptible individuals. These data imply that relative resistance to L. morhua exists in cod, that it is heritable, and that broodstock selection could be used to limit the impact of microsporidian infections on growth during finfish aquaculture.