Evaluating the Potential Fitness Effects of Chinook Salmon (Oncorhynchus tshawytscha) Aquaculture Using Non-Invasive Population Genomic Analyses of MHC Nucleotide Substitution Spectra

SIMPLE SUMMARY: DNA sequence variation in the major histocompatibility complex (MHC) is vital to the health of the vertebrate adaptive immune system. Consequently, MHC Class I and II loci have evolved to become the most polymorphic vertebrate genes known. This extraordinary level of variation makes MHC immunity genes both prime indicators of individual fitness as well as highly sensitive biomarkers for assessing the population genetic health of wildlife, and by extension, sustainable management of biodiversity. We examined levels of MHC locus-specific DNA haplotype variation in both wild and hatchery-reared Chinook salmon (Oncorhynchus tshawytscha) sampled from the Susitna River Basin where wild Alaskan Chinook stocks are declining regionally and creating incentives for expanded aquaculture. Our non-invasive population analyses indicated higher levels of observed heterozygosity than expected heterozygosity at the Class I and II loci and minimal genetic differentiation between spatially distinct subpopulations. Class I sequences also showed evidence of balancing selection, despite high rates of non-synonymous substitutions observed, specifically at the peptide binding regions of both MHC genes. Taken together, these results suggest that current management practices for Chinook populations in the Susitna Basin are not likely causing any detrimental biological changes in salmon in relation to immune health. Moreover, the immune health of the hatchery fish, at least in the context of the two populations studied, matches that of the wild fish. Our locus-specific work invites a genome-wide survey such as mapping Single Nucleotide Polymorphisms to better understand the role of the MHC in optimal mate choice and to establish MHC relatedness as a proxy for maintaining genetic variability throughout the entire genomes of fish within populations. ABSTRACT: Genetic diversity plays a vital role in the adaptability of salmon to changing environmental conditions that can introduce new selective pressures on populations. Variability among local subpopulations may increase the chance that certain advantageous genes are passed down to future generations to mitigate susceptibility to novel diseases, warming oceans, loss of genetic stocks, and ocean acidification. Class I and II genes of the major histocompatibility complex (MHC) are crucial for the fitness of Chinook salmon due to the role they play in disease and pathogen resistance. The objective of this study was to assess the DNA sequence variability among wild and hatchery populations of Alaskan Chinook salmon at the class I α1 and class II β1 exons of the MHC. We hypothesized that the 96 wild samples taken from the Deshka River would display greater levels of observed heterozygosity (Ho) relative to expected heterozygosity (He) in suggesting that individuals with similar phenotypes mate with one another more frequently than would be expected under random mating patterns. Conversely, since no mate selection occurs in the William Jack Hernandez Sport Fish hatchery, we would not expect to see this discrepancy (He = Ho) in the 96 hatchery fish tested in this study. Alternatively, we hypothesized that post-mating selection is driving higher levels of observed heterozygosity as opposed to mate selection. If this is the case, we will observe higher than expected levels of heterozygosity among hatchery salmon. Both populations displayed higher levels of observed heterozygosity than expected heterozygosity at the Class I and II loci but genetic differentiation between the spatially distinct communities was minimal. Class I sequences showed evidence of balancing selection, despite high rates of non-synonymous substitutions observed, specifically at the peptide binding regions of both MHC genes.