Adaptive genetic markers discriminate migratory runs of Chinook salmon (Oncorhynchus tshawytscha) amid continued gene flow

Abstract

Neutral genetic markers are routinely used to define distinct units within species that warrant discrete management. Human-induced changes to gene flow however may reduce the power of such an approach. We tested the efficiency of adaptive versus neutral genetic markers in differentiating temporally divergent migratory runs of Chinook salmon (Oncorhynchus tshawytscha) amid high gene flow owing to artificial propagation and habitat alteration. We compared seven putative migration timing genes to ten microsatellite loci in delineating three migratory groups of Chinook in the Feather River, CA: offspring of fall-run hatchery broodstock that returned as adults to freshwater in fall (fall run), spring-run offspring that returned in spring (spring run), and fall-run offspring that returned in spring (FRS). We found evidence for significant differentiation between the fall and federally listed threatened spring groups based on divergence at three circadian clock genes (OtsClock1b, OmyFbxw11, and Omy1009UW), but not neutral markers. We thus demonstrate the importance of genetic marker choice in resolving complex life history types. These findings directly impact conservation management strategies and add to previous evidence from Pacific and Atlantic salmon indicating that circadian clock genes influence migration timing.

Temporal dynamics of migration‐linked genetic variation are driven by streamflows and riverscape permeability

“…Our result that a migration‐linked trait does not lead to neutral genetic divergence parallels results from diverse systems, from birds to fish (Bensch, Åkesson, & Irwin, ; O’Malley, Camara, & Banks, ; O’Malley et al, ). Migration is often linked to a narrow region in the genome (Liedvogel, Åkesson, & Bensch, ), and is often associated with dramatic phenotypic changes in migrating individuals.…”

“…Landscape features can shape both neutral genetic structure and the distribution of adaptive variation within a species (Davis, Epps, Flitcroft, & Banks, ; Grummer et al, ; Orsini, Andrew, & Eizaguirre, ). While landscape genetic studies in rivers increasingly consider adaptive variation (Brauer, Unmack, Smith, Bernatchez, & Beheregaray, ; Micheletti, Matala, Matala, & Narum, ; Vincent, Dionne, Kent, Lien, & Bernatchez, ), few studies have directly compared patterns of neutral genetic variation with patterns of variation at loci associated with adaptive phenotypic variation (but see Hand et al, ; Keller, Taverna, & Seehausen, ; O’Malley, Jacobson, Kurth, Dill, & Banks, ). This comparison could improve our understanding of the mechanisms that either facilitate or restrict gene flow in the face of selection and adaptive divergence on life history characteristics (e.g., migratory vs. resident life histories) in fragmented river networks and landscapes.…”

Identification of multiple genetically distinct populations of Chinook salmon (Oncorhynchus tshawytscha) in a small coastal watershed

“…Timing of freshwater entry and reproductive maturity in salmonid fishes is a complex array of interrelated behavioral and physiological traits that has heritable components and exhibits phenotypic plasticity in response to environmental variability (Carlson and Seamons 2008;Abadia-Cardoso et al 2013). Chinook salmon populations have been able to exploit a wide range of habitats because of evolution at this trait, often in the face of ongoing gene flow (Waples 2001;O'Malley et al 2013). Using markers associated with the circadian clock gene network might have provided additional insight in the differentiation among these closely related groups and they did discriminate the spring-run population above the waterfall from all downstream fish, although with genetic differentiation similar to the other markers.…”

Evolution of phenology in a salmonid population: a potential adaptive response to climate change

“…The precision with which salmonids time migration can constrain gene flow between seasonally distinct spawning segments, thereby enabling local adaptation of phenology (Quinn et al 2000;Fillatre et al 2003;Gharrett et al 2013). Evidence of local adaptation of phenology in salmonids has been provided by comparisons of seasonally distinct groups of Chinook salmon (Oncorhynchus tshawytscha) that spawn in the same river, which demonstrated significant genetic divergence at three circadian clock genes, but not at neutral markers (O'Malley et al 2013). The tight coupling of salmonid ecology and phenology, along with the generally high heritability of phenological traits in salmonids (median h 2 = 0.51; Carlson and Seamons 2008), suggests that salmonid populations may respond to periodic environmental fluctuations or persistent climatic trends through contemporary evolution of phenology.…”