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Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream-resident (fluvial), lake-migrant (adfluvial) and ocean-migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site-associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.

Humans by their very nature alter the distribution of species. Be it introduction of exotic species, habitat alterations or construction of barriers, anthropogenic changes provide novel experimental systems for the molecular ecologist to study evolutionary change. These events often provide a contradiction. Effective population sizes are generally low, and introduced populations are typically characterized by reduced diversity consistent with theoretical predictions of population bottlenecks and founder effects. However, despite reduced diversity, rapid change sometimes occurs. Identification of genomic regions associated with these rapid adaptive responses to novel selection pressures provides a window into genomic regions important in adaptive diversity, both in the novel and native ranges. These studies also provide an important means to estimate the pace of evolutionary change. In this issue, Willoughby et al. () compared the heterozygosity of steelhead (the anadromous form of rainbow trout Oncorhynchus mykiss) introduced into Lake Michigan in the late 1880s to the putative source population from the ancestral California range. After 25 generations of isolation in Lake Michigan, Willoughby et al. () found consistent genomewide reductions in genetic diversity as estimated by a measure of pooled heterozygosity. Despite this overall reduction in heterozygosity, three chromosomal regions showed signals of rapid adaptation and contained genes associated with osmoregulatory and wound-healing functions.

Understanding the genetic mechanisms that facilitate adaptive radiation is an important component of evolutionary biology. Here, we genotyped 82 neutral SNPs, seven SNPs in islands of divergence identified in a previous study (island SNPs), and a region of the major histocompatibility complex (MHC) in 32 populations of sockeye salmon to investigate whether conserved genes and genomic regions are involved in adaptive radiation. Populations representing three ecotypes were sampled from seven drainages with differing habitats and colonization histories spanning a range of 2,000 km. We found strong signatures of parallel selection across drainages at the island SNPs and MHC, suggesting that the same loci undergo divergent selection during adaptive radiation. However, patterns of differentiation at most island SNPs and the MHC were not associated with ecotypes, suggesting that these loci are responding differently to a mosaic of selective pressures. Our study provides some of the first evidence that conserved genomic islands may be involved in adaptive divergence of salmon populations. Additionally, our data provide further support for the hypothesis that sockeye salmon inhabiting rivers unconnected to lakes harbour similar genetic diversity across large distances, are likely the ancestral form of the species, and have repeatedly recolonized lake systems as they have become available after glacial recession. Finally, our results highlight the value and importance of validating outlier loci by screening additional populations and regions, a practice that will hopefully become more common in the future.

Puritz et al. provide a review of several RADseq methodological approaches in response to our 'Population Genomic Data Analysis' workshop (Sept 2013) review (Andrews & Luikart 2014). We agree with Puritz et al. on the importance for researchers to thoroughly understand RADseq library preparation and data analysis when choosing an approach for answering their research questions. Some of us are currently using multiple RADseq protocols, and we agree that the different methods may offer advantages in different cases. Our workshop review did not intend to provide a thorough review of RADseq because the workshop covered a broad range of topics within the field of population genomics. Similarly, neither the response of Puritz et al. nor our comments here provide sufficient space to thoroughly review RADseq. Nonetheless, here we address some key points that we find unclear or potentially misleading in their evaluation of techniques.

Numerous empirical studies have reported lack of migration–drift equilibrium in wild populations. Determining the causes of nonequilibrium population structure is challenging because different evolutionary processes acting at a variety of spatiotemporal scales can produce similar patterns. Studies of contemporary populations in northern latitudes suggest that nonequilibrium population structure is probably caused by recent colonization of the region after the last Pleistocene ice age ended ~13 000 years ago. The chum salmon's (Oncorhynchus keta) range was fragmented by dramatic environmental changes during the Pleistocene. We investigated the population structure of chum salmon on the North Alaska Peninsula (NAP) and, using both empirical data and simulations, evaluated the effects of colonization timing and founder population heterogeneity on patterns of genetic differentiation. We screened 161 single nucleotide polymorphisms and found evidence of nonequilibrium population structure when the slope of the isolation-by-distance relationship was examined at incremental spatial scales. In addition, simulations suggested that this pattern closely matched models of recent colonization of the NAP by secondary contact. Our results agree with geological and archaeological data indicating that the NAP was a dynamic landscape that may have been more recently colonized than during the last deglaciation because of dramatic changes in coastal hydrology over the last several thousand years.

A whole genome duplication (WGD) doubles the entire genomic content of a species and is thought to have catalyzed adaptive radiation in some polyploid-origin lineages. However, little is known about general consequences of a WGD since gene duplicates (i.e. paralogs) are commonly filtered in genomic studies; such filtering may remove substantial portions of the genome in data sets from polyploid-origin species. We demonstrate a new method that enables genome-wide scans for signatures of selection at both non-duplicated and duplicated loci by taking locus-specific copy number into account. We apply this method to RAD sequence data from different ecotypes of a polyploid-origin salmonid (Oncorhynchus nerka) and reveal signatures of divergent selection that would have been missed if duplicated loci were filtered. We also find conserved signatures of elevated divergence at pairs of homeologous chromosomes with residual tetrasomic inheritance suggesting that joint evolution of some non-diverged gene duplicates may affect the adaptive potential of these genes. These findings illustrate that including duplicated loci in genomic analyses enables novel insights into the evolutionary consequences of WGDs and local segmental gene duplications. This article is protected by copyright. All rights reserved.

Whole-genome duplications are major evolutionary events with a lasting impact on genome structure. Duplication events complicate genetic analyses as paralogous sequences are difficult to distinguish; consequently, paralogs are often excluded from studies. The effects of an ancient whole-genome duplication (approximately 88 MYA) are still evident in salmonids through the persistence of numerous paralogous gene sequences and partial tetrasomic inheritance. We use restriction site-associated DNA sequencing on 10 collections of chum salmon from the Salish Sea in the USA and Canada to investigate genetic diversity and population structure in both tetrasomic and rediploidized regions of the genome. We use a pedigree and high-density linkage map to identify paralogous loci and to investigate genetic variation across the genome. By applying multivariate statistical methods, we show that it is possible to characterize paralogous loci and that they display similar patterns of population structure as the diploidized portion of the genome. We find genetic associations with the adaptively important trait of run-timing in both sets of loci. By including paralogous loci in genome scans, we can observe evolutionary signals in genomic regions that have routinely been excluded from population genetic studies in other polyploid-derived species.

Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes, contrasting neutral structure throughout the rest of the genome which was low and not partitioned by ecotype. One island on linkage group 13 was particularly large and contained six SNPs with FST > 0.14 (average FST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a non-synonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80 - 402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking, however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation. This article is protected by copyright. All rights reserved.

Single nucleotide polymorphisms (SNPs) are a class of genetic markers that are well suited to a broad range of research and management applications. Although advances in genotyping chemistries and analysis methods continue to increase the potential advantages of using SNPs to address molecular ecological questions, the scarcity of available DNA sequence data for most species has limited marker development. As the number and diversity of species being targeted for large-scale sequencing has increased, so has the potential for using sequence from sister taxa for marker development in species of interest. We evaluated the use of Oncorhynchus mykiss and Salmo salar sequence data to identify SNPs in three other species (Oncorhynchus tshawytscha, Oncorhynchus nerka and Oncorhynchus keta). Primers designed based on O. mykiss and S. salar alignments were more successful than primers designed based on Oncorhynchus-only alignments for sequencing target species, presumably due to the much larger number of potential targets available from the former alignments and possibly greater sequence conservation in those targets. In sequencing approximately 89 kb we observed a frequency of 4.30 x 10(-3) SNPs per base pair. Approximately half (53/101) of the subsequently designed validation assays resulted in high-throughput SNP genotyping markers. We speculate that this relatively low conversion rate may reflect the duplicated nature of the salmon genome. Our results suggest that a large number of SNPs could be developed for Pacific salmon using sequence data from other species. While the costs of DNA sequencing are still significant, these must be compared to the costs of using other marker classes for a given application.

The genes of the major histocompatibility complex (MHC) are an important component of the vertebrate immune system and can provide insights into the role of pathogen-mediated selection in wild populations. Here, we examined variation at the MHC class II peptide-binding region in 27 populations of sockeye salmon (Oncorhynchus nerka), distributed among three distinct spawning ecotypes, from a complex of interconnected rivers and lakes in south-western Alaska. We also obtained genotypes from 90 putatively neutral single nucleotide polymorphisms for each population to compare the relative roles of demography and selection in shaping the observed MHC variation. We found that MHC divergence was generally partitioned by spawning ecotype (lake beaches, rivers and streams) and was 30 times greater than variation at neutral markers. Additionally, we observed substantial differences in modes of selection and diversity among ecotypes, with beach populations displaying higher levels of directional selection and lower MHC diversity than the other two ecotypes. Finally, the level of MHC differentiation in our study system was comparable to that observed over much larger geographic ranges, suggesting that MHC variation does not necessarily increase with increasing spatial scale and may instead be driven by fine-scale differences in pathogen communities or pathogen virulence. The low levels of neutral structure and spatial proximity of populations in our study system indicate that MHC differentiation can be maintained through strong selective pressure even when ample opportunities for gene flow exist.

Studying the effect of similar environments on diverse genetic backgrounds has long been a goal of evolutionary biologists with studies typically relying on experimental approaches. Pink salmon, a highly abundant and widely ranging salmonid, provide a naturally occurring opportunity to study the effects of similar environments on divergent genetic backgrounds due to a strict two-year semelparous life history. The species is composed of two reproductively isolated lineages with overlapping ranges that share the same spawning and rearing environments in alternate years. We used restriction-site-associated DNA (RAD) sequencing to discover and genotype approximately 8000 SNP loci in three population pairs of even- and odd-year pink salmon along a latitudinal gradient in North America. We found greater differentiation within the odd-year than within the even-year lineage and greater differentiation in the southern pair from Puget Sound than in the northern Alaskan population pairs. We identified 15 SNPs reflecting signatures of parallel selection using both a differentiation-based method (BAYESCAN) and an environmental correlation method (BAYENV). These SNPs represent genomic regions that may be particularly informative in understanding adaptive evolution in pink salmon and exploring how differing genetic backgrounds within a species respond to selection from the same natural environment.

Given over 90 combined years in academic and professional activities related to genetics and fishery management (FU 57, JS 36—see Waples et al. 2008), we are pleased to provide an invited perspective generated by the interesting and useful article of McCusker & Bentzen (2010). These authors reaffirm the apparent signature of neutrality of mitochondrial and microsatellite markers through an exhaustive analysis of archived genotypic data for 105 marine and freshwater fishes. They note that their conclusions are consistent with earlier and less comprehensive analyses and that they do not exclude the operation of some selective activity (e.g. genetic ‘draft’), which may be overwhelmed by Ne-related stochastic processes. Here, we provide a complementary focus, recalling relevant issues related to neutrality and selection in applications of molecular variations in fishery management.

Single nucleotide polymorphisms (SNPs) are a class of genetic markers that are well suited to a broad range of research and management applications. Although advances in genotyping chemistries and analysis methods continue to increase the potential advantages of using SNPs to address molecular ecological questions, the scarcity of available DNA sequence data for most species has limited marker development. As the number and diversity of species being targeted for large-scale sequencing has increased, so has the potential for using sequence from sister taxa for marker development in species of interest. We evaluated the use of Oncorhynchus mykiss and Salmo salar sequence data to identify SNPs in three other species (Oncorhynchus tshawytscha, Oncorhynchus nerka and Oncorhynchus keta). Primers designed based on O. mykiss and S. salar alignments were more successful than primers designed based on Oncorhynchus-only alignments for sequencing target species, presumably due to the much larger number of potential targets available from the former alignments and possibly greater sequence conservation in those targets. In sequencing approximately 89 kb we observed a frequency of 4.30 x 10(-3) SNPs per base pair. Approximately half (53/101) of the subsequently designed validation assays resulted in high-throughput SNP genotyping markers. We speculate that this relatively low conversion rate may reflect the duplicated nature of the salmon genome. Our results suggest that a large number of SNPs could be developed for Pacific salmon using sequence data from other species. While the costs of DNA sequencing are still significant, these must be compared to the costs of using other marker classes for a given application.