Host-pathogen-environment interactions determine survival outcomes of adult sockeye salmon (Oncorhynchus nerka) released from fisheries

Stressful environments enhance the pathogenicity of infectious agents. But can pathogens decrease host stressor resilience? We tested the hypothesis that enhanced infections reduce the resilience of wild adult sockeye salmon (Oncorhynchus nerka) to single and cumulative stressors. To manipulate initial infections, some returning adults were collected in the marine environment prior to entering the Fraser River, British Columbia, and another group was collected after freshwater entry. Fish were held in freshwater tanks for up to 4 weeks at historical (14°C) or projected future migration temperatures (18°C). The cumulative impact of fisheries non-retention was evaluated by exposing fish to a mild (seine) or severe (gill net) fishery treatment at collection. Using weekly nonlethal gill biopsies and high-throughput qPCR, we measured up to 46 infectious agents with host stress and immune gene expression. Marine-captured fish had less severe infections than river-captured fish: a short migration (100 km, 5-7 d) that produced profound infection differences. At 14°C, river-captured fish survived 1-2 weeks less than marine captured fish. All fish held at 18°C died within 4 weeks unless they were not handled, and few river-captured fish survived. Gene expression correlated with infections in river-captured fish, while marine-captured fish were more stressor-responsive. Our results implicate river-derived infections as causal factors of stressor-mediated early mortality in migrating adult sockeye salmon, whereas cumulative stressors were detrimental regardless of initial infections due to extreme physiological disturbance. We propose that river entry decreases stressor resilience of adult Pacific salmon by shifting infections and redirecting host responses toward disease resistance.