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Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring.

ABSTRACT: The Atlantic herring (Clupea harengus), one of the most abundant marine fishes in the world, has historically been a critical food source in Northern Europe. It is one of the few marine species that can reproduce throughout the brackish salinity gradient of the Baltic Sea. Previous studies based on few genetic markers have revealed a conspicuous lack of genetic differentiation between geographic regions, consistent with huge population sizes and minute genetic drift. Here, we present a cost-effective genome-wide study in a species that lacks a genome sequence. We first assembled a muscle transcriptome and then aligned genomic reads to the transcripts, creating an "exome assembly," capturing both exons and flanking sequences. We then resequenced pools of fish from a wide geographic range, including the Northeast Atlantic, as well as different regions in the Baltic Sea, aligned the reads to the exome assembly, and identified 440,817 SNPs. The great majority of SNPs showed no appreciable differences in allele frequency among populations; however, several thousand SNPs showed striking differences, some approaching fixation for different alleles. The contrast between low genetic differentiation at most loci and striking differences at others implies that the latter category primarily reflects natural selection. A simulation study confirmed that the distribution of the fixation index F(ST) deviated significantly from expectation for selectively neutral loci. This study provides insights concerning the population structure of an important marine fish and establishes the Atlantic herring as a model for population genetic studies of adaptation and natural selection.

SUBMITTER: Lamichhaney S

PROVIDER: S-EPMC3511109 | biostudies-literature | 2012 Nov

REPOSITORIES: biostudies-literature

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Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring.

Lamichhaney Sangeet S Martinez Barrio Alvaro A Rafati Nima N Sundström Görel G Rubin Carl-Johan CJ Gilbert Elizabeth R ER Berglund Jonas J Wetterbom Anna A Laikre Linda L Webster Matthew T MT Grabherr Manfred M Ryman Nils N Andersson Leif L

Proceedings of the National Academy of Sciences of the United States of America 20121107 47

The Atlantic herring (Clupea harengus), one of the most abundant marine fishes in the world, has historically been a critical food source in Northern Europe. It is one of the few marine species that can reproduce throughout the brackish salinity gradient of the Baltic Sea. Previous studies based on few genetic markers have revealed a conspicuous lack of genetic differentiation between geographic regions, consistent with huge population sizes and minute genetic drift. Here, we present a cost-effe ...[more]

PMID: 23134729

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Project description:BackgroundElucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations.ResultsWe generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used FST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees.ConclusionsDespite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.

Project description:The Atlantic herring Clupea harengus L has a vast geographical distribution and a complex population structure with a few very large migratory units and many small local populations. Each population has its own spawning ground and/or time, thereby maintaining their genetic integrity. Several herring populations migrate between common feeding grounds and over-wintering areas resulting in frequent mixing of populations. Thus, many herring fisheries are based on mixed populations of different demographic status. In order to avoid over-exploitation of weak populations and to conserve biodiversity, understanding the population structure and population mixing is important for maintaining biologically sustainable herring fisheries. The aim of this study was to investigate the genetic population structure of herring in the Faroese and surrounding waters, and to develop genetic markers for distinguishing between four herring management units (often called stocks), namely the Norwegian spring-spawning herring (NSSH), Icelandic summer-spawning herring (ISSH), North Sea autumn-spawning herring (NSAH), and Faroese autumn-spawning herring (FASH). Herring from the four stocks were sequenced at low coverage, and single nucleotide polymorphisms (SNPs) were called and used for population structure analysis and individual assignment. An ancestry-informative SNP panel with 118 SNPs was developed and tested on 240 individuals. The results showed that all four stocks appeared to be genetically differentiated populations, but at lower levels of differentiation between FASH and ISSH than the other two populations. Overall assignment rate with the SNP panel was 80.7%, and agreement between the genetic and traditional visual assignment was 75.5%. The NSAH and NSSH samples had the highest assignment rate (100% and 98.3%, respectively) and highest agreement between traditional and genetic assignment methods (96.6% and 94.9%, respectively). The FASH and ISSH samples had substantially lower assignment rates (72.9% and 51.7%, respectively) and agreement between traditional and genetic methods (39.5% and 48.4%, respectively).

Project description:The introduction of Next Generation Sequencing (NGS) has revolutionised population genetics, providing studies of non-model species with unprecedented genomic coverage, allowing evolutionary biologists to address questions previously far beyond the reach of available resources. Furthermore, the simple mutation model of Single Nucleotide Polymorphisms (SNPs) permits cost-effective high-throughput genotyping in thousands of individuals simultaneously. Genomic resources are scarce for the Atlantic herring (Clupea harengus), a small pelagic species that sustains high revenue fisheries. This paper details the development of 578 SNPs using a combined NGS and high-throughput genotyping approach. Eight individuals covering the species distribution in the eastern Atlantic were bar-coded and multiplexed into a single cDNA library and sequenced using the 454 GS FLX platform. SNP discovery was performed by de novo sequence clustering and contig assembly, followed by the mapping of reads against consensus contig sequences. Selection of candidate SNPs for genotyping was conducted using an in silico approach. SNP validation and genotyping were performed simultaneously using an Illumina 1,536 GoldenGate assay. Although the conversion rate of candidate SNPs in the genotyping assay cannot be predicted in advance, this approach has the potential to maximise cost and time efficiencies by avoiding expensive and time-consuming laboratory stages of SNP validation. Additionally, the in silico approach leads to lower ascertainment bias in the resulting SNP panel as marker selection is based only on the ability to design primers and the predicted presence of intron-exon boundaries. Consequently SNPs with a wider spectrum of minor allele frequencies (MAFs) will be genotyped in the final panel. The genomic resources presented here represent a valuable multi-purpose resource for developing informative marker panels for population discrimination, microarray development and for population genomic studies in the wild.

Dataset Information

Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring.

Publications

Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring.

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