Genomewide association analyses of fitness traits in captive-reared Chinook salmon: Applications in evaluating conservation strategies

Abstract

A novel application of genomewide association analyses is to use trait-associated loci to monitor the effects of conservation strategies on potentially adaptive genetic variation. Comparisons of fitness between captive- and wild-origin individuals, for example, do not reveal how captive rearing affects genetic variation underlying fitness traits or which traits are most susceptible to domestication selection. Here, we used data collected across four generations to identify loci associated with six traits in adult Chinook salmon (Oncorhynchus tshawytscha) and then determined how two alternative management approaches for captive rearing affected variation at these loci. Loci associated with date of return to freshwater spawning grounds (return timing), length and weight at return, age at maturity, spawn timing, and daily growth coefficient were identified using 9108 restriction site-associated markers and random forest, an approach suitable for polygenic traits. Mapping of trait-associated loci, gene annotations, and integration of results across multiple studies revealed candidate regions involved in several fitness-related traits. Genotypes at trait-associated loci were then compared between two hatchery populations that were derived from the same source but are now managed as separate lines, one integrated with and one segregated from the wild population. While no broad-scale change was detected across four generations, there were numerous regions where trait-associated loci overlapped with signatures of adaptive divergence previously identified in the two lines. Many regions, primarily with loci linked to return and spawn timing, were either unique to or more divergent in the segregated line, suggesting that these traits may be responding to domestication selection. This study is one of the first to utilize genomic approaches to demonstrate the effectiveness of a conservation strategy, managed gene flow, on trait-associated-and potentially adaptive-loci. The results will promote the development of trait-specific tools to better monitor genetic change in captive and wild populations.

Keywords: captive rearing; conservation; domestication selection; genomewide association analysis; managed gene flow; random forest.

Figure 1

Schematic illustrating the initiation (the founding P ₁ generation) and subsequent propagation (F ₁–F ₄ generations) of the integrated and segregated hatchery lines of anadromous Chinook salmon at the Cle Elum Supplementation and Research Facility (modified from Waters et al., 2015). Each box denotes the number of spawners (wild environment) and the number of broodstock (hatchery environment) for each year surveyed. Linear arrows indicate the contribution of wild spawners or hatchery broodstock to the subsequent generation. Circular arrows represent unobserved mating between wild‐born (unmarked) and hatchery‐born (marked) spawners in the wild environment. Fish from the two lines are differentially marked, so only hatchery‐born fish from the integrated line are permitted to spawn in the wild. Dark gray boxes represent wild adults, light gray boxes represent natural‐origin adults with hatchery, wild, or hybrid ancestry, and white boxes represent adults born in the hatchery

Figure 2

Graphical representation of four Chinook salmon chromosomes (center panels, a–d) showing the map positions (cM) of loci associated with six fitness‐related traits, as identified by random forest analyses. Loci associated with different traits mapped to the same regions, including loci on Ots01 and Ots08 that were associated with both fork length and weight (highlighted in yellow). Divergence (F _ST) of the F ₃ INT and F ₃ SEG hatchery lines when compared to the P ₁ founders is displayed in the left and right panels of each figure, respectively. The F ₃ generation is shown because it is the most recent hatchery generation for which there are relatively large sample sizes (>50), and thus has greater statistical support for all outlier tests. The black line denotes the moving average of F _ST across the chromosome, with regions exhibiting significant levels of divergence (i.e., outlier regions) from the P ₁ Founders in red (Waters et al., 2015, 2017). The centromere of each chromosome is shaded with diagonal black lines. Black circles represent outlier loci previously identified by F _TEMP and Bayescan, blue triangles correspond to trait‐associated loci, and gray points are all other study loci. Locations where trait‐associated loci are in close proximity to outlier loci or regions are marked with black arrows, including one outlier locus on Ots10 that was also associated with spawn timing (circled)

Figure 3

Loci and regions of chromosome Ots12 showing signatures of adaptive divergence based on measures of pairwise F _ST between each generation of each line and the P ₁ founders. The results are given for the integrated (top panel) and segregated (bottom panel) hatchery lines through the F ₁, F ₂, F ₃, and F ₄ generations. Blue squares are loci that were identified as outliers by Bayescan (Foll & Gaggiotti, 2008) and orange triangles are outliers identified by F _TEMP, a method designed to detect selection in a single population over time (Therkildsen et al., 2013). The red line represents the kernel‐smoothed moving average of F _ST, and the gray shaded area is the 95% confidence interval. Genomic regions exhibiting significant levels of divergence (i.e., outlier regions) from the P ₁ founders occur where the moving average of F _ST exceeds the 95% confidence intervals. The centromere of the chromosome is shaded with diagonal black lines. The black circle designates a locus predictive of return timing, Ot005185_Ots12p, which was also identified as an outlier by Bayescan and, in the segregated line, by F _TEMP. Negative F _ST values occur due to finite sample sizes and slight variance in sample sizes between populations (Weir & Cockerham, 1984)