Genomic divergence of hatchery- and natural-origin Chinook salmon (Oncorhynchus tshawytscha) in two supplemented populations

Abstract

Captive propagation is widely used for the conservation of imperiled populations. There have been concerns about the genetic effects of such propagation, but few studies have measured this directly at a genomic level. Here, we use moderate-coverage (10X) genome sequences from 80 individuals to evaluate the genomic distribution of variation of several paired groups of Chinook salmon (Oncorhynchus tshawytscha). These include 1) captive and natural-origin sh separated by at least one generation, 2) sh within the same generation having high tness in captivity compared to those with high tness in the wild, and 3) sh listed as different Evolutionarily Signi cant Units (ESUs) under the US Endangered Species Act. The distribution of variation between high tness captive and high tness natural sh was nearly identical to that expected from random sampling, indicated that differential selection in the two environments did not create large allele frequency differences within a single generation. In contrast, the samples from distinct ESUs were clearly more divergent than expected by chance, including a peak of divergence near the GREB1L gene on chromosome 28, a gene previously associated with variation in time of return to fresh water. Comparison of hatchery and natural-origin sh within a population fell between these extremes, but the maximum value of F ST was similar to the maximum between ESUs, including a peak of divergence on chromosome 8 near the slc7a2 and pdgfrl genes. These results suggest that efforts at limiting genetic divergence between captive and natural sh in these populations have successfully kept the average divergence low across the genome, but at a small portion of their genomes, hatchery and natural salmon were as distinct as individuals from different ESUs.

Genomic evidence for domestication selection in three hatchery populations of Chinook salmon, Oncorhynchus tshawytscha

“…The identified outlier peaks are relatively narrow (3-158 kb) compared to those identified in many other studies of local adaptation (Clucas et al, 2019;Duranton et al, 2018;Ford et al, 2023;Thompson et al, 2020). This is especially true when compared to F ST peaks found in systems with high gene flow, where blocks of high differentiation and low recombination often span megabases (Clucas et al, 2019;Huang et al, 2020;Via, 2012).…”

“…Recently, Ford et al. ( 2023 ) used whole‐genome sequencing to investigate domestication in spring‐run Chinook salmon from the Upper Columbia River and documented a peak of divergence between hatchery and wild populations on Ots08. Interestingly, this peak was near a locus associated with spawn timing documented in Waters et al.…”

“…While phenotypic differences between hatchery and wild salmon are consistently reported and widely accepted (Naish et al., 2007 ), the causative genetic basis and the corresponding genetic repeatability across independent hatchery–wild population pairs remain unresolved. Most genomic regions found to differ across hatchery and wild salmon have been specific to the study system (Ford et al., 2023 ; Waters et al., 2015 , 2018 ). In Chinook salmon, Waters et al.…”

“…While phenotypic differences between hatchery and wild salmon are consistently reported and widely accepted (Naish et al, 2007), the causative genetic basis and the corresponding genetic repeatability across independent hatchery-wild population pairs remain unresolved. Most genomic regions found to differ across hatchery and wild salmon have been specific to the study system (Ford et al, 2023;Waters et al, 2015Waters et al, , 2018. In Chinook salmon, Waters et al (2015Waters et al ( , 2018 observed that the genetic divergence of a segregated hatchery population from the founding wild population increased with each additional generation of hatchery rearing due to the combined effects of drift and domestication selection.…”

“…Furthermore, the authors identified specific loci that diverged across consecutive generations of hatchery-rearing and linked some of these loci to fitness-related traits such as spawn timing, suggesting that genetic and phenotypic effects of domestication can occur at rapid timescales (Waters et al, 2015(Waters et al, , 2018. In addition, a wholegenome sequencing study on Chinook salmon identified divergence between hatchery and wild fish after at least one generation in captivity (Ford et al, 2023). These studies provide insightful genetic comparisons of wild and hatchery Pacific salmon, but it remains unclear if the genetic pathways of domestication selection are consistent across hatcheries.…”