Christopher Habicht

Summer-Fall Distribution of Stocks of Immature Sockeye Salmon in the Bering Sea as Revealed by Single-Nucleotide Polymorphisms

Abstract We report stock composition estimates for immature (ocean-age .1 and .2) sockeye salmon Oncorhynchus nerka distributed across the Bering Sea in late summer and fall. We establish a baseline data set composed of single-nucleotide polymorphism markers that can achieve very high accuracies in identifying sockeye salmon stocks from throughout their range in Asia and North America. We demonstrate the capabilities of this data set to address high-seas salmon issues by analyzing samples collected by researchers from Russia, Japan, and the United States during late summer and fall 2002–2004 as part of the Bering–Aleutian Salmon International Survey. According to our findings, (1) Gulf of Alaska (GOA) stocks formed a significant portion of the immature sockeye salmon migrating in the eastern and central Bering Sea in summer and fall, and western GOA stocks had a broader distribution in the Bering Sea than eastern GOA stocks; (2) Asian stocks migrated as far east as the western Aleutian Islands and the Don...

Single-Nucleotide Polymorphisms (SNPs) under Diversifying Selection Provide Increased Accuracy and Precision in Mixed-Stock Analyses of Sockeye Salmon from the Copper River, Alaska

Abstract Genetic markers are increasingly being used to ascertain the population of origin of individuals or mixtures of individuals in complex aggregations of Pacific salmon Oncorhynchus spp. Multilocus genotype data from single-nucleotide polymorphisms (SNPs) are especially useful for admixture analyses. Single-nucleotide polymorphisms can be discovered in nonmodel organisms with relative ease and can be characterized in the coding and regulatory regions of the genome influenced by selection. Those influenced by diversifying selection may show atypically high levels of differentiation among populations and thus be particularly valuable for genetic stock identification in cases where neutral loci show little difference among populations of interest. We identified four SNP loci from a panel of 42 as candidates for diversifying selection (referred to here as nonneutral SNPs) in sockeye salmon O. nerka from the Copper River and adjacent coastal drainages in south-central Alaska. We evaluated the information...

Spawning Habitat and Geography Influence Population Structure and Juvenile Migration Timing of Sockeye Salmon in the Wood River Lakes, Alaska

Abstract The strict homing of sockeye salmon Oncorhynchus nerka results in reproductively isolated populations that often spawn in close proximity and share rearing habitat. High spawning fidelity enables these populations to adapt to local conditions, resulting in a wide range of life history characteristics and genetic variation within individual watersheds. The Wood River system in southwestern Alaska provides a pristine, well-studied system in which to examine fine-scale population structure and its influences on juvenile life histories. Adult sockeye salmon spawn in lake beaches, rivers, and small tributaries throughout this watershed, and juveniles rear in five nursery lakes. We genotyped 30 spawning populations and 6,066 migrating smolts at 45 single nucleotide polymorphism loci, two of which are candidates for positive selection in the study system. We show that there is significant genetic structure (F ST = 0.032) in the Wood River lakes and that divergence is generally related to spawning rather...

Multiplex preamplification PCR and microsatellite validation enables accurate single nucleotide polymorphism genotyping of historical fish scales.

Incorporating historical tissues into the study of ecological, conservation and management questions can broaden the scope of population genetic research by enhancing our understanding of evolutionary processes and anthropogenic influences on natural populations. Genotyping historical and low‐quality samples has been plagued by challenges associated with low amounts of template DNA and the potential for pre‐existing DNA contamination among samples. We describe a two‐step process designed to (i) accurately genotype large numbers of historical low‐quality scale samples in a high‐throughput format and (ii) screen samples for pre‐existing DNA contamination. First, we describe how an efficient multiplex preamplification PCR of 45 single nucleotide polymorphisms (SNPs) can generate highly accurate genotypes with low failure and error rates in subsequent SNP genotyping reactions of individual historical scales from sockeye salmon (Oncorhynchus nerka). Second, we demonstrate how the method can be modified for the amplification of microsatellite loci to detect pre‐existing DNA contamination. A total of 760 individual historical scale and 182 contemporary fin clip samples were genotyped and screened for contamination. Genotyping failure and error rates were exceedingly low and similar for both historical and contemporary samples. Pre‐existing contamination in 21% of the historical samples was successfully identified by screening the amplified microsatellite loci. The advantages of automation, low failure and error rates, and ability to multiplex both the preamplification and subsequent genotyping reactions combine to make the protocol ideally suited for efficiently genotyping large numbers of potentially contaminated low‐quality sources of DNA.

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

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.

Genetic and Ecological Divergence Defines Population Structure of Sockeye Salmon Populations Returning to Bristol Bay, Alaska, and Provides a Tool for Admixture Analysis

Abstract We examined the population genetic diversity and structure of sockeye salmon Oncorhynchus nerka spawning in tributaries of Bristol Bay, Alaska, a region that supports the largest commercial fisheries for sockeye salmon in the world. Genetic variation among the sockeye salmon populations, as revealed by microsatellite data, was shallower than that found in other areas of comparable size around the Pacific Rim. This finding was driven by similarity among populations rearing in the four largest lake systems located on the southeastern side of the bay (upper and lower Ugashik, Becharof, Naknek–Grosvenor–Coville, and Iliamna lakes). Sockeye salmon in lakes located above known obstacles to migration on the southeastern side and in tributaries on the northwestern side showed variation and structure that were more typical of the species. Management of these important fisheries assumes knowledge of the composition of stock mixtures captured in each fishery. We investigated the potential of microsatellite ...

Smaller effective population sizes evidenced by loss of microsatellite alleles in tributary-spawning populations of sockeye salmon from the Kvichak River, Alaska drainage

We tested signals of historical reductions in effective population size within populations of sockeye salmon Oncorhynchus nerka returning to Bristol Bay, Alaska, to examine the roles that ecotype, migration obstacles, and drainage might play in the highly variable production of the Kvichak River drainage. We collected data for eight microsatellite loci from ∼100 fish at each of 16 locations within the Kvichak River drainage and five locations within the more productively stable Naknek River drainage. Pair-wise exact tests were used to group similar collections within ecotype, within drainage, and above and below migration obstacles. After grouping, collections represented independent populations for further analyses. We examined the number of alleles per locus, mean ratio of the number of alleles to the range in allele size, heterozygosity excess, and gametic disequilibrium as measures of reduction-in-population-size events. Number of alleles per locus revealed the largest number of significant differences. Tributary populations showed a stronger signal consistent with reduced effective population size than did beach populations within the Kvichak River drainage. Kvichak River drainage populations showed a stronger signal consistent with reduced effective population size than did the Naknek River drainage populations. Populations above migration obstacles showed signals consistent with reduction in historical population sizes in multiple measures indicating some of these reductions may be severe enough to qualify as demographic bottlenecks.

Single-Nucleotide Polymorphic Genotypes Reveal Patterns of Early Juvenile Migration of Sockeye Salmon in the Eastern Bering Sea

Abstract We estimate patterns of nearshore migration in the eastern Bering Sea for out-migrating Bristol Bay sockeye salmon Oncorhynchus nerka in their first year at sea. Over 3,000 juveniles were collected during the late summer of 2005–2007 as part of the Bering–Aleutian Salmon International Survey and tested with a regional genetic baseline of 45 single-nucleotide polymorphisms. Population-specific and westward migrations from natal rivers were evident. Populations from Wood River and northwestward predominated in the northern latitudes of Bristol Bay and the eastern Bering Sea and populations from the Egegik River and southwestward in the southern latitudes, while the populations spawning at the head of Bristol Bay had the highest proportions in the middle latitudes. These patterns were stable across years, apparently unaffected by marine productivity and temperature. This continuum of marine migratory patterns most likely reflects stable and population-specific adaptations to buffer the distribution ...

Coded wire tag placement affects homing ability of pink salmon

Abstract Coded wire tags (CWTs) are routinely injected into the snouts of Pacific salmon Oncorhynchus spp. as fry to estimate contributions of tagged populations to spawning escapements and near-shore fisheries and to assess straying. Because not all fish are tagged, tag recoveries are extrapolated to include contributions of nontagged fish released at the same time and location. A key assumption in the extrapolations is that CWTs do not affect homing ability and therefore migratory pathways. We studied tag position within the heads of homing and straying adult pink salmon O. gorbuscha returning to Prince William Sound, Alaska, to test the hypothesis that poor tag position induces straying. Heads from straying and homing tagged adults were recovered in 1992 and 1994 and X-rayed. Tag locations were categorized into critical and noncritical areas, based on tag position relative to olfactory organs and nerves. In 1992, the 37 analyzed pink salmon that strayed were more likely to have tags in critical positio...

Source-Sink Estimates of Genetic Introgression Show Influence of Hatchery Strays on Wild Chum Salmon Populations in Prince William Sound, Alaska

The extent to which stray, hatchery-reared salmon affect wild populations is much debated. Although experiments show that artificial breeding and culture influence the genetics of hatchery salmon, little is known about the interaction between hatchery and wild salmon in a natural setting. Here, we estimated historical and contemporary genetic population structures of chum salmon (Oncorhynchus keta) in Prince William Sound (PWS), Alaska, with 135 single nucleotide polymorphism (SNP) markers. Historical population structure was inferred from the analysis of DNA from fish scales, which had been archived since the late 1960’s for several populations in PWS. Parallel analyses with microsatellites and a test based on Hardy-Weinberg proportions showed that about 50% of the fish-scale DNA was cross-contaminated with DNA from other fish. These samples were removed from the analysis. We used a novel application of the classical source-sink model to compare SNP allele frequencies in these archived fish-scales (1964–1982) with frequencies in contemporary samples (2008–2010) and found a temporal shift toward hatchery allele frequencies in some wild populations. Other populations showed markedly less introgression, despite moderate amounts of hatchery straying. The extent of introgression may reflect similarities in spawning time and life-history traits between hatchery and wild fish, or the degree that hybrids return to a natal spawning area. The source-sink model is a powerful means of detecting low levels of introgression over several generations.