Remnant salmon life history diversity rediscovered in a highly compressed habitat

Chinook salmon (Oncorhynchus tshawytscha) display remarkable life history diversity underpinning their ability to adapt to environmental change. Maintaining life history diversity is vital to the resilience and stability of Chinook salmon metapopulations, particularly under rapidly changing climates. However, the conditions that promote life history diversity are rapidly disappearing, as anthropogenic forces promote homogenization of habitats and genetic lineages. In this study, we use the highly modified Yuba River in California to understand if distinct genetic lineages and life history still exist, despite reductions in spawning habitat and hatchery practices that have promoted introgression. There currently is a concerted effort to protect federally listed spring run populations, given that few wild populations still exist. Despite this, we lack a comprehensive understanding of the genetic and life history diversity of Chinook salmon present in the Yuba River system. To understand this diversity, we collected migration timing data and GREB1L genotypes from hook-and-line, acoustic tagging, and carcass surveys of Chinook salmon in the Yuba River between 2009-2011. Variation in the GREB1L region of the genome is tightly linked with run timing in Chinook salmon throughout the range, but the relationship between this variation and entry on spawning grounds is little explored in the Central Valley. We found that the date Chinook salmon crossed the lowest barrier to Yuba River spawning habitat (Daguerre Point Dam) was tightly correlated with their GREB1L genotype. Importantly, our study confirms that ESA-listed spring run Chinook salmon are spawning in the Yuba River, promoting a portfolio of life history and genetic diversity, despite spawning in a compressed habitat. This work highlights the need to identify and protect this life history diversity in heavily impacted systems to maintain healthy Chinook salmon metapopulations in those systems. Without this, we run the risk of losing the last vestiges of important variation.

Methods
Samples were collected through three main sampling efforts, a hook-and-line survey, an acoustic telemetry project, and a carcass survey, conducted by the RMT between the years 2009-2011 as part of their annual surveys to characterize Chinook salmon migration up the Yuba River to the spawning reaches. For the hook-and-line survey and acoustic telemetry effort, genetic samples were collected from all adult fish caught via hook-and-line sampling, targeting fish in the lowermost reaches from the confluence of the Yuba and Feather Rivers to DPD from May to October, 6 days a week during the years 2010-2011. Fin clips were collected from all captured fish (N=122), but only fish that were determined to be in “good condition” (showing no signs of disease or injury) were selected to be acoustically tagged as part of the acoustic tagging survey effort (N=42, we refer to these as the “acoustic tagging samples'' and those that were just fin clipped but not tagged as “hook-and-line survey samples''). The acoustic tagging samples were tagged with VEMCO V13-1L acoustic transmitters via esophageal/gastric insertion and were detected via two ultrasonic receivers located in the north and south side of the top of the fish ladder to detect fish successfully passing DPD from both sides (PSMFC, 2011; VEMCO, 2010). The most upstream area was sampled via carcass surveys that occurred upstream of the DPD on a weekly basis during the years 2009-2010, starting 10-15 days after the first spawning redds were detected each year. Only fresh carcasses (possessing at least one clear eye and gills that are red or pink) were sampled to avoid sampling fish that had degraded DNA and had already been in the system for a long period of time. In 2009 and 2010, tissue samples were taken from carcasses throughout the river reach between the DPD and Englebright Dam.

To genotypically assign run-type, we extracted DNA from fin clips using the DNeasy® Blood and Tissue extraction kit (Qiagen, Valencia, CA). We genotyped fish at a specific region of GREB1L previously shown to be the most highly associated with Chinook salmon run timing in Central Valley populations (Thompson et al 2020) by selecting five Single Nucleotide Polymorphisms (SNPs) across this region that had been identified as strongly associated with run timing in previous analyses (Koch and Narum, 2020; Thompson et al., 2020).