Increased mitochondrial DNA diversity in ancient Columbia River basin Chinook salmon Oncorhynchus tshawytscha

Abstract

The Columbia River and its tributaries provide essential spawning and rearing habitat for many salmonid species, including Chinook salmon (Oncorhynchus tshawytscha). Chinook salmon were historically abundant throughout the basin and Native Americans in the region relied heavily on these fish for thousands of years. Following the arrival of Europeans in the 1800s, salmon in the basin experienced broad declines linked to overfishing, water diversion projects, habitat destruction, connectivity reduction, introgression with hatchery-origin fish, and hydropower development. Despite historical abundance, many native salmonids are now at risk of extinction. Research and management related to Chinook salmon is usually explored under what are termed "the four H's": habitat, harvest, hatcheries, and hydropower; here we explore a fifth H, history. Patterns of prehistoric and contemporary mitochondrial DNA variation from Chinook salmon were analyzed to characterize and compare population genetic diversity prior to recent alterations and, thus, elucidate a deeper history for this species. A total of 346 ancient and 366 contemporary samples were processed during this study. Species was determined for 130 of the ancient samples and control region haplotypes of 84 of these were sequenced. Diversity estimates from these 84 ancient Chinook salmon were compared to 379 contemporary samples. Our analysis provides the first direct measure of reduced genetic diversity for Chinook salmon from the ancient to the contemporary period, as measured both in direct loss of mitochondrial haplotypes and reductions in haplotype and nucleotide diversity. However, these losses do not appear equal across the basin, with higher losses of diversity in the mid-Columbia than in the Snake subbasin. The results are unexpected, as the two groups were predicted to share a common history as parts of the larger Columbia River Basin, and instead indicate that Chinook salmon in these subbasins may have divergent demographic histories.

Fig 1. Locations discussed in the study.

Ancient sample locations for the Columbia (1–3), Snake (6–8), and Spokane (5) sample groups are indicated with black circles. Contemporary sample locations for the Columbia (near 4) and Snake (near 9) are indicated with blue lines.

Fig 2. Haplotype networks of ancient and contemporary groups, including Columbia sub-groups.

Orientation for haplotypes is constant between networks, circle size is proportional to frequency in the grouping, lines represent mutational connections. Four “evolutionary backbone” types as defined by Martin et al. [42]are labeled for reference in the network.

Fig 3. Three-dimensional, temporal haplotype network for all Columbia River samples.

Circle sizes are proportional to relative haplotype frequencies, horizontal lines represent single mutation connections between haplotypes.

Fig 4. Bayesian cladogram for Chinook haplotypes from full species range, as well as novel haplotypes detected in this study.

Previously identified types are coded according to geographic region north: blue, central: yellow, southern: red per designations in Martin et al. [42]. All novel types fell into shared geographic clades (Northern/Central or Central/Southern).

Fig 5. Extended Bayesian skyline plots (EBSPs) for Columbia and Snake River groups (A) and rate of reduction in Nef indicated in the associated EBSP (B).

Mean effective population size is indicated with solid black line, median with dashed line, and 95% highest posterior density (HPD) in shaded grey. Contrasting patterns are present for the two groups; the Columbia River groups visually indicates a reduction in mean effective population size while no such reduction is present for Snake River samples.

Fig 6. Comparison of spatial (top) and temporal (lower four) haplotype sampling.

Orientation for haplotypes is constant between networks, circle size is proportional to frequency in the grouping, lines represent mutational connections. Spatial network (top) is color coded for: southern-red, central-yellow, and northern-blue portions of the species range. No association between haplotypes and climate periods is noted.