Genetic signals of artificial and natural dispersal linked to colonization of South America by non‐native Chinook salmon (Oncorhynchus tshawytscha)

Abstract

Genetics data have provided unprecedented insights into evolutionary aspects of colonization by non‐native populations. Yet, our understanding of how artificial (human‐mediated) and natural dispersal pathways of non‐native individuals influence genetic metrics, evolution of genetic structure, and admixture remains elusive. We capitalize on the widespread colonization of Chinook salmon Oncorhynchus tshawytscha in South America, mediated by both dispersal pathways, to address these issues using data from a panel of polymorphic SNPs. First, genetic diversity and the number of effective breeders (N b) were higher among artificial than natural populations. Contemporary gene flow was common between adjacent artificial and natural and adjacent natural populations, but uncommon between geographically distant populations. Second, genetic structure revealed four distinct clusters throughout the Chinook salmon distributional range with varying levels of genetic connectivity. Isolation by distance resulted from weak differentiation between adjacent artificial and natural and between natural populations, with strong differentiation between distant Pacific Ocean and Atlantic Ocean populations, which experienced strong genetic drift. Third, genetic mixture analyses revealed the presence of at least six donor geographic regions from North America, some of which likely hybridized as a result of multiple introductions. Relative propagule pressure or the proportion of Chinook salmon propagules introduced from various geographic regions according to government records significantly influenced genetic mixtures for two of three artificial populations. Our findings support a model of colonization in which high‐diversity artificial populations established first; some of these populations exhibited significant admixture resulting from propagule pressure. Low‐diversity natural populations were likely subsequently founded from a reduced number of individuals.

Mixed-stock analyses among migratory, non-native Chinook salmon at-sea and assignment to natal sites in freshwater at their introduced range in South America

“…Toltén River supports one of the largest Chinook salmon populations identified to-date in Chile (Gomez-Uchida et al 2018). The entire watershed comprises four lakes and multiple rivers that run from the Andean mountains to the Pacific Ocean (Figure 1a).…”

“…We screened DNA samples through a suite of 170 SNPs (Table S1). These loci were selected based on information content among non-native populations, fit to Hardy-Weinberg equilibrium (HWE) proportions, and non-significant linkage disequilibrium (LD) among loci (Gomez-Uchida et al 2018). We calculated genetic statistics, expected heterozygosities and allelic richness, for all three groups of samples using GENEPOP (Rousset 2008).…”

“…We built a set of reference populations from Chinook salmon genotypes (n=504) including six Pacific Ocean and two Atlantic Ocean watershed sites in South America (Gomez-Uchida et al 2018; Figure 1c). Multilocus genotypes at 170 SNPs (Table S1) originated from collections of juvenile and spawners taken from natal sites in freshwater.…”

“…Genotypes were bootstrapped by resampling alleles following Anderson et al (2008) in 200 mixtures per natal site containing 100 individuals each. Highly admixed genotypes (possibly hybrids; Gomez-Uchida et al 2018) were removed from the database, because in simulations they assigned to two or more reference populations. Third, we used Bayesian assignment (Rannala, Mountain 1997) to estimate membership probabilities of one estuary and two coastal Chinook salmon mixtures to reference populations using ONCOR.…”

“…The clear fishery potential of Chinook salmon triggered government-sponsored and private initiatives to successfully propagate it throughout Pacific Ocean watersheds in South America during 1978-1990 (Correa, Gross 2008), with donor (native) populations spanning multiple geographic regions from North America (Correa, Moran 2017; Gomez-Uchida et al 2018; Riva Rossi et al 2012). A recent genetics study has shown that non-native Chinook salmon have invaded new watersheds in South America establishing genetically differentiated population groups originating from both artificial and natural dispersal (Gomez-Uchida et al 2018). Genetically isolated populations can be useful as reference groups to understand migratory behavior and identifying natal populations among mixed stock salmonids at sea (Bellinger et al 2015; Bradbury et al 2016; McKinney et al 2017).…”