Single nucleotide polymorphisms unravel hierarchical divergence and signatures of selection among Alaskan sockeye salmon (Oncorhynchus nerka) populations

Abstract

BackgroundDisentangling the roles of geography and ecology driving population divergence and distinguishing adaptive from neutral evolution at the molecular level have been common goals among evolutionary and conservation biologists. Using single nucleotide polymorphism (SNP) multilocus genotypes for 31 sockeye salmon (Oncorhynchus nerka) populations from the Kvichak River, Alaska, we assessed the relative roles of geography (discrete boundaries or continuous distance) and ecology (spawning habitat and timing) driving genetic divergence in this species at varying spatial scales within the drainage. We also evaluated two outlier detection methods to characterize candidate SNPs responding to environmental selection, emphasizing which mechanism(s) may maintain the genetic variation of outlier loci.ResultsFor the entire drainage, Mantel tests suggested a greater role of geographic distance on population divergence than differences in spawn timing when each variable was correlated with pairwise genetic distances. Clustering and hierarchical analyses of molecular variance indicated that the largest genetic differentiation occurred between populations from distinct lakes or subdrainages. Within one population-rich lake, however, Mantel tests suggested a greater role of spawn timing than geographic distance on population divergence when each variable was correlated with pairwise genetic distances. Variable spawn timing among populations was linked to specific spawning habitats as revealed by principal coordinate analyses. We additionally identified two outlier SNPs located in the major histocompatibility complex (MHC) class II that appeared robust to violations of demographic assumptions from an initial pool of eight candidates for selection.ConclusionsFirst, our results suggest that geography and ecology have influenced genetic divergence between Alaskan sockeye salmon populations in a hierarchical manner depending on the spatial scale. Second, we found consistent evidence for diversifying selection in two loci located in the MHC class II by means of outlier detection methods; yet, alternative scenarios for the evolution of these loci were also evaluated. Both conclusions argue that historical contingency and contemporary adaptation have likely driven differentiation between Kvichak River sockeye salmon populations, as revealed by a suite of SNPs. Our findings highlight the need for conservation of complex population structure, because it provides resilience in the face of environmental change, both natural and anthropogenic.

Homing of Sockeye Salmon within Hidden Lake, Alaska, Can Be Used to Achieve Hatchery Management Goals

“…Importantly, both explanations indicate homing behavior within a small lake system. Natural populations of stream and lake spawning Sockeye Salmon are thought to home to natal sites with some precision (Groot and Margolis 1991;Hendry et al 1996;Quinn et al 1999;Gomez-Uchida et al 2011), so that genetic differences between spawning populations might be expected. However, genetic differences among spawning groups of Sockeye Salmon within a lake were not observed in three Bristol Bay lakes (Varnavskaya et al 1994;Habicht et al 2007), in three lakes in Cook Inlet (Burger et al 1995;Seeb et al 2000), and in one of the two lakes in Russia (Varnavskaya et al 1994).…”

“…This homing behavior isolates spawning groups so that random genetic drift and local selection produce differences among groups, which can often be detected with molecular markers (Grant et al 1980;Hendry et al 1996Hendry et al , 2000Seeb et al 2000). Although lake and stream spawners often differ genetically, less variation among spawning groups occurs within lakes (Varnavskaya et al 1994;Burger et al 1995;Seeb et al 2000;Habicht et al 2007;Gomez-Uchida et al 2011).…”

Understanding the adaptive consequences of hatchery-wild interactions in Alaska salmon

“…On a regional scale, MHC allele-frequency differentiation was similar to microsatellite differentiation, but selective forces within river systems tended to produce greater MHC than microsatellite differentiation (Landry and Bernatchez 2001). In Alaska, similar geographic and temporal MHC allele-frequency variability has been observed in populations of sockeye salmon around Bristol Bay (Gomez-Uchida et al 2011). Together, these studies show the association between genetic and environmental variation.…”

Landscape heterogeneity and local adaptation define the spatial genetic structure of Pacific salmon in a pristine environment

“…The two sockeye salmon MHC SNPs are found in one exon (One_MHC2_190) and one intron (One_MHC2_251) within a Major Histocompatibility Complex (MHC) class II gene (Miller and Withler 1996;Miller et al 2001;Limborg et al 2011). Several studies support the adaptive nature of MHC polymorphisms related to pathogen-mediated selection (Dionne et al 2009;Evans and Neff 2009;McGlauflin et al 2011;Gomez-Uchida et al 2011). Differences in the spawning and rearing habitats (i.e.…”

“…The lake ecotype is the typical form of sockeye salmon that spends about half its life in a nursery lake before emigrating to the marine environment to mature, whereas the sea/river ecotype is a rarer form that rears in the freshwater environment for a much shorter and more variable period of time. Large differences in MHC allele frequencies between geographically proximate populations of the two ecotypes have been observed elsewhere throughout the range of sockeye salmon (Creelman et al 2011;Gomez-Uchida et al 2011;McGlauflin et al 2011). The two sockeye salmon MHC SNPs are found in one exon (One_MHC2_190) and one intron (One_MHC2_251) within a Major Histocompatibility Complex (MHC) class II gene (Miller and Withler 1996;Miller et al 2001;Limborg et al 2011).…”