Evidence of disruption in estrogen-associated signaling in the liver transcriptome of in-migrating sockeye salmon of British Columbia, Canada

Abstract

The health of sockeye (Oncorhynchus nerka) salmon stocks is of increasing concern; reflecting both a sentinel of human-impacted aquatic environments and as a key fishery for British Columbia, Canada. The spawning migration of Pacific sockeye salmon represents a critical life stage where significant demands are made on animal biology and important BC fisheries are linked to this migration in the Skeena and Fraser River watersheds. These watersheds present very different environments; the former being sparsely populated with little industrial impact, while the latter flows through highly-populated areas. The present study used quantitative real-time PCR analysis of adult sockeye salmon from four 2008 stocks [Fulton River and Pinkut Creek (Skeena) and Weaver Creek and Harrison River (Fraser)] to evaluate ten hepatic gene transcripts associated with reproduction, stress, energy metabolism, and exposure to environmental contaminants. Dynamic changes in mRNA abundance were observed in Fulton River stock animals from the Skeena River mouth to the spawning ground which reflect the physiological demands of in-river migration and reproductive maturation. Inter-stock comparisons of migrants at spawning grounds demonstrated a marked difference in the sex-specific gene hepatic gene expression profiles. Our original hypothesis was that a greater diversity in mRNA profiles is associated with watersheds with higher human impact. However, our observations contradict this posit. Skeena males and females displayed poor definition in their molecular profiles between sexes while the Fraser River fish had very distinctive sex differences that were consistent with the previous year's migration. The genetic sex distribution and ratio of milt versus roe production did not differ between the Skeena and Fraser River spawning site fish. However, a significant percentage of Skeena animals displayed marked discordance of these characteristics with gender-specific hepatic mRNA profiles implying that an alteration in estrogen-mediated signaling has occurred. Continued geospatial and longitudinal assessments will help determine to what extent the dynamic molecular biology of late life-stage sockeye salmon reflects natural variation or modulation by anthropogenic causative agents.