In a nutshell

• Chinook salmon exhibit “spring-run” or “fall-run” migration timing in many parts of the species’ range, an adaptation that permits spawning during different periods of the year as a means of minimizing the risk of adverse conditions or facilitating access to spawning grounds upstream of natural barriers like waterfalls
• Although fall-run populations remain generally healthy, spring-run populations have declined markedly over the past century due to anthropogenic impacts and because the spring-run lifecycle often involves fish remaining in freshwater for extended periods before spawning
• Analysis of changes in Chinook genetic structure over time indicates that human impacts on watersheds have induced a shift in the relative frequency of spring-run and fall-run alleles at a single locus, with negative implications for Chinook phenotypic variation and adaptive potential
• The spring-run allele has not been preserved in fall-run populations at levels sufficient to ensure natural recovery of the spring-run phenotype, and thus recovery of the spring-run phenotype may hinge on conservation of the few extant spring-run populations

Adult Chinook salmon (Oncorhynchus tshawytscha) engage in two seasonal upstream migrations to spawning grounds: the fall run, which typically occurs in late summer through autumn, and the spring run, which may begin as early as March and continues into early summer. Whether an adult Chinook migrates in the spring or in the fall is a behavioral trait based on differences in a single gene, and as such the “spring-run” and “fall-run” populations compose two distinct Chinook phenotypes and genotypes. At the population and species levels, such temporal variation in spawning is an important adaptive strategy because it spreads reproduction over different times of the year, reducing the risk of the reproductive effort being impaired by adverse environmental conditions. In addition, maintenance of phenotypic variation is critical for a species’ ability to cope with changes in its environment.

Although both Chinook phenotypes are vulnerable to human impacts on watersheds, fall-run populations remain relatively robust throughout most of the species’ range. Spring-run populations, in contrast, have been reduced to a mere fraction of their historical abundance, and are currently on the brink of extinction in (or have already disappeared from) many watersheds along the Pacific coast. This disparity in the effect that human activities have had on the relative abundance of the two phenotypes can be attributed primarily to differences in their lifecycles: fall-run phenotypes are sexually mature and spawn more or less immediately upon arrival at suitable sites, and therefore spend a minimal amount of time in streams and rivers, whereas spring-run phenotypes migrate upstream before reaching maturity and may fast for weeks prior to spawning, which reduces their fitness and extends their exposure to poor water quality and toxins.

Because phenotypic variation is vital to a species’ ability to adapt to changing environmental conditions, the marked reduction in spring-run phenotype abundance may have dire implications for Chinook salmon as human impacts intensify and climate change accelerates over the coming decades. It was this concern that led Tasha Thompson, a doctoral candidate at the University of California, Davis, and colleagues to undertake a critical examination of what effects human activities are having on the genetic diversity – and thus the adaptive potential – of Chinook populations. To do so, they first collected fish from watersheds in Oregon and California where spring-run populations still occur, including the Rogue River in Oregon. Prior to construction of the Lost Creek Dam in 1977, Chinook spawning in the Rogue system took place primarily in spring, but spring-run populations rapidly declined following dam construction; today, fall-run Chinook are now the main spawners in the Rogue watershed. Thompson and her team determined that the shift in reproductive timing from spring to autumn corresponded with a shift in the proportional frequency of alleles at a single locus, with spring-run alleles now far less common in the wider gene pool of the Rogue population.

DNA extracted from salmon bones retrieved from Indigenous middens and other archaeological sites along the length of California’s Klamath River – a watershed that no longer supports spring runs due to the presence of numerous dams – was then used to compare historical allelic frequency to current proportions in populations of Chinook that still spawn in several Klamath tributaries. This analysis revealed that while spring-run allelic frequency was high in ancient Klamath Chinook, indicating the former presence of a healthy spring-run population, spring-run genes are extremely infrequent in present-day fall-run populations; indeed, less than 1% of fall-run fish carry the spring-run allele. As such, the authors concluded, fall-run populations are unlikely to serve as adequate genetic reservoirs for the spontaneous recovery of spring-run populations, even in fully restored watersheds.

Thompson et al.’s study shows that anthropogenic impacts have driven wide-scale loss of spring-run Chinook populations along the Pacific coast of North America, with potentially disastrous implications for the species’ ability to adapt to future environmental change. Moreover, the scarcity of the spring-run allele in fall-run populations makes natural recovery of spring-run populations highly improbable. Future recovery of the spring-run Chinook phenotype – and the species’ adaptive potential – thus poses a significant management and conservation challenge, as watershed restoration efforts alone will be insufficient for promoting the re-emergence of populations of spring-run Chinook salmon in the rivers and streams where they were formerly abundant.

Science Spotlight by Ken Ferguson

More salmon science in the news:

• California WaterBlog: Evolutionary Genomics Informs Salmon Conservation
• UC Davis: Human Actions Impact Wild Salmon’s Ability to Evolve