Genetic evidence for ecological divergence in kokanee salmon

Abstract

The evolution of locally adapted phenotypes among populations that experience divergent selective pressures is a central mechanism for generating and maintaining biodiversity. Recently, the advent of high-throughput DNA sequencing technology has provided tools for investigating the genetic basis of this process in natural populations of nonmodel organisms. Kokanee, the freshwater form of sockeye salmon (Oncorhynchus nerka), occurs as two reproductive ecotypes, which differ in spawning habitat (tributaries vs. shorelines); however, outside of the spawning season the two ecotypes co-occur in many lakes and lack diagnostic morphological characteristics. We used restriction site-associated DNA (RAD) sequencing to identify 6145 SNPs and genotype kokanee from multiple spawning sites in Okanagan Lake (British Columbia, Canada). Outlier tests revealed 18 loci putatively under divergent selection between ecotypes, all of which exhibited temporally stable allele frequencies within ecotypes. Six outliers were annotated to sequences in the NCBI database, two of which matched genes associated with early development. There was no evidence for neutral genetic differentiation; however, outlier loci demonstrated significant structure with respect to ecotype and had high assignment accuracy in mixed composition simulations. The absence of neutral structure combined with a small number of highly divergent outlier loci is consistent with theoretical predictions for the early stages of ecological divergence. These outlier loci were then applied to a realistic fisheries scenario in which additional RAD sequencing was used to genotype kokanee collected by trawl in Okanagan Lake, providing preliminary evidence that this approach may be an effective tool for conservation and management.

An ancient selective sweep linked to reproductive life history evolution in sockeye salmon

“…29 15Shuswap LakeEagle RiverBritish Columbia, CanadaFraserKokaneeStream90.28Taylor et al . 29 16Skaha LakeOkanagan RiverBritish Columbia, CanadaColumbiaSockeyeStream330.02Veale & Russello 71 17Penticton ChannelBritish Columbia, CanadaColumbiaKokaneeStream190.08Veale & Russello 71 18Okanagan LakeOkanagan LakeBritish Columbia, CanadaColumbiaKokaneeShore1440.99Lemay & Russello 59 Mission CreekBritish Columbia, CanadaColumbiaKokaneeStream1360.10Lemay & Russello 59 19Wood LakeWood LakeBritish Columbia, CanadaColumbiaKokaneeShore480.92Frazer & Russello 42 Middle Vernon CreekBritish Columbia, CanadaColumbiaKokaneeStream480.28Frazer & Russello 42 20Kalmalka LakeKalmalka LakeBritish Columbia, CanadaColumbiaKokaneeShore320.95Veale & Russello 71 Coldstream CreekBritish Columbia, CanadaColumbiaKokaneeStream320.23Veale & Russello 71 21Christina LakeChristina LakeBritish Columbia, CanadaColumbiaKokaneeShore481.00Frazer 70 Sanders CreekBritish Columbia, CanadaColumbiaKokaneeStream480.07Frazer 70 22…”

“…As sockeye salmon are unique among the Pacific salmonids in their flexibility to spawn in lake-shore benthic environments 31 , this region provides great promise for future investigations of the genomic basis of O. nerka life history evolution, and more broadly, for increasing our understanding of the heritable basis of adaptation of complex traits in novel environments. From an applied perspective, this highly informative SNP has immediate utility for informing fisheries management throughout British Columbia 59 and likely across the entire range.…”

Transcriptome sequencing reveals both neutral and adaptive genome dynamics in a marine invader

“…; Moore et al . ), and reveals the relative contributions of neutral and adaptive processes to differentiation between populations (Lemay & Russello ).…”

Genetic Stock Identification Reveals That Angler Harvest Is Representative of Cryptic Stock Proportions in a High‐Profile Kokanee Fishery

“…; Frazer and Russello ; Lemay and Russello ; Veale and Russello , , b). Importantly, the incorporation of outlier loci within genotyping panels has greatly improved the accuracy and precision of individual assignment and mixed‐composition analyses for management of kokanee (Lemay and Russello , ; Russello et al. ; Frazer and Russello ; Veale and Russello ), and other freshwater and marine species (Freamo et al.…”

“…In the case of kokanee, the application of population genomic techniques has allowed for the identification of outlier loci that are associated with reproductive ecotypes in a number of lakes throughout British Columbia and elsewhere across their distribution (Russello et al. ; Frazer and Russello ; Lemay and Russello ; Veale and Russello , , b). Importantly, the incorporation of outlier loci within genotyping panels has greatly improved the accuracy and precision of individual assignment and mixed‐composition analyses for management of kokanee (Lemay and Russello , ; Russello et al.…”