Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci
- Department of Medical Biochemistry and Microbiology, Uppsala University, Sweden
- Department of Veterinary Integrative Biosciences, Texas A&M University, United States
- National Institute of Aquatic Resources, Technical University of Denmark, Denmark
- Department of Biological Sciences, University of Bergen, Norway
- Institute of Marine Research, Norway
- Department of Aquatic Resources, Institute of Marine Research, Swedish University of Agricultural Sciences, Sweden
- Department of Biological, Geological and Environmental Sciences, University of Bologna, Italy
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Ireland
- Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Sweden
Figures
Figure 1 with 1 supplement
Geographic distribution of sampled pools of Atlantic herring.
Color code of each population refers to the spawning season that a given pool was sampled.
Figure 1—figure supplement 1
Variation in sea water temperatures among seasons.
Seasonal sea water temperature profiles across the North Atlantic and the Baltic Sea. Herring sampling locations are overlaid on top of the temperature data. Climatic data layers at a 0.25° spatial …
Figure 2 with 3 supplements
Principal component analysis (PCA) of herring populations.
(a) PCA based on 169,934 genetically undifferentiated markers. (b) PCA based on 794 markers that are likely under natural selection. Color of each population represents spawning season, as coded in F…
Figure 2—figure supplement 1
Phylogenetic reconstruction.
(a) Neighbor-joining tree of 53 Atlantic herring populations based on allele frequency of genome-wide SNPs. (b) Geographical distribution of populations in relation to phylogenetic clustering. Color …
Figure 2—figure supplement 2
Pairwise FST among 53 populations of Atlantic herring.
Figure 2—figure supplement 3
Histogram of genome-wide standard deviation of allele frequencies across 52 Atlantic and Baltic populations.
We selected 22,195 undifferentiated markers and 794 markers that are likely under natural selection based on the cutoffs (SD <0.02 and SD >0.2).
Figure 3 with 4 supplements
Genetic signals associated with ecological adaptation.
(a) Genetic differentiation between superpools of Baltic and Atlantic herring in spring- spawners (above) and in autumn-spawners (below) and (b) a zoomed-in profile for Chr12. (c) Genetic …
Figure 3—figure supplement 1
Genetic differentiation between superpools of Atlantic and Baltic herring in spring-spawners (above the x-axis) and autumn-spawners (below the x-axis).
Results for individual chromosomes. SNPs with raw p>10−30 in both spring and autumn-spawners are colored in grey. SNPs with raw raw p<10−30 in both spring and autumn-spawners are colored in red …
Figure 3—figure supplement 2
Genetic differentiation around (a) PRLR gene and (b) SOX11B gene in each contrast.
Raw p-values are presented here and adjusted p-values are given in Supplementary files 4 an5, respectively.
Figure 3—figure supplement 3
Genetic differentiation between super-pools of spring and autumn-spawning herring in Atlantic (above) and in Baltic herring (below).
Results for individual chromosomes. SNPs with raw p>10−30 in both spring and autumn-spawners are colored in grey. SNPs with raw p<10−30 in both spring and autumn-spawners are colored in red while …
Figure 3—figure supplement 4
Comparisons of p-values and delta allele frequencies (DAF) for the contrasts shown in Figure 3.
For each contrast used, the same three sub-panels are shown. i: a QQ-plot of observed vs. expected –log10(P)-values, where the red line is a line with slope one and the black line represents a …
Figure 4 with 5 supplements
Genetic differentiation between herring populations from Ireland and Britain vs.other populations from the Northeast Atlantic.
(a) Putative structural variants on Chr6, 12, 17 and 23 are indicated with red stars. (b to e) are zoomed-in profiles on the corresponding chromosomes. Strong genetic differentiation is observed in …
Figure 4—figure supplement 1
Allele frequency of diagnostic SNPs at four putative structural variants across populations of Atlantic herring and one Pacific outgroup.
Figure 4—figure supplement 2
Heatmap of the genotypes for diagnostic SNPs based on individual whole-genome sequencing data at four putative structural variants.
Figure 4—figure supplement 3
Frequencies of two estimated haplotypes in each population at four putative structural variants on Chr6 (a), Chr12 (b), Chr17 (c), and Chr23 (d) across the geographical distribution.
Figure 4—figure supplement 4
Neighbor-joining tree based on genotypes of all SNPs in each of the four putative structural variants respectively on Chr6 (a), Chr12 (b), Chr17 (c), and Chr23 (d).
Average nucleotide diversity was estimated for S and N haplotypes in each tree.
Figure 4—figure supplement 5
Comparisons of p-values and delta allele frequencies (DAF) for the contrast shown in Figure 4.
(a) A QQ-plot of observed vs. expected –log10(P)-values, where the red line is a line with slope one and the black line represents a linear regression using the first (i.e. least significant) 90% of …
Figure 5 with 3 supplements
Genetic differentiation between Atlantic herring from the North Atlantic vs. waters around Ireland, Britain, and the transition zone.
(a) Genome-wide screen. (b) Genetic differentiation on Chr2 and a zoom-in profile of the AHR2B2 locus. Red dots refer to the four missense mutations.
Figure 5—figure supplement 1
The missense mutation (Ser346Thr) in AHR2B2 and a multi-species amino acid alignment of AHR sequences across vertebrate species.
There are four isoforms of AHR in herring organized as two gene pairs: AHR1B2-AHR2B2 on chromosome two and AHR1B1-AHR2B1 on chromosome 21. These have been named based on sequence similarity to the Ah…
Figure 5—figure supplement 2
Heatmap of allele frequencies based on pooled samples for SNPs in the interval 6.35 Mb to 6.37 Mb on chromosome 19 with absolute delta allele frequencies above 0.4 in the contrast shown in Figure 5.
The color side-bar indicates the frequency of the reference allele, and the top bar highlights (in purple) the one non-synonymous SNP in the set: chr19_6359267. This polymorphism causes a missense …
Figure 5—figure supplement 3
Comparisons of p-values and delta allele frequencies (DAF) for the contrast shown in Figure 5.
(a) A QQ-plot of observed vs. expected –log10(P)-values, where the red line is a line with slope one and the black line represents a linear regression using the first (i.e. least significant) 90% of …
Figure 6
PacBio long reads defining inversion breakpoints on chromosomes 6 and 17.
(a) Chromosome 6. The orientation of an informative read is indicated with arrows above the Chr6 reference panel. The breakpoints are indicated with dotted blue lines. The region just outside the …
Author response image 1
Additional files
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Supplementary file 1
Specimen information of 53 pooled samples.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp1-v2.xlsx
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Supplementary file 2
Specimen information of 55 individual sequencing samples.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp2-v2.xlsx
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Supplementary file 3
Definition of how superpools were formed by pooling population samples of major groups of herring.
Sample names correspond to those given in Supplementary file 1.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp3-v2.xlsx
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Supplementary file 4
List of SNPs showing strong genetic differentiation between superpools of Atlantic and Baltic herring.
The criteria for inclusion was raw p<10−30 for both comparisons (among spring-spawners and among autumn-spawners) or raw p<10−50 for a single comparison. These are the SNPs colored in red or black in Figure 3—figure supplement 1. Raw p-values are given in columns E and G and corrected p-values in columns F and H.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp4-v2.xlsx
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Supplementary file 5
List of loci showing strong genetic differentiation between superpools of spring and autumn-spawning herring.
The criteria for inclusion was raw p<10−30 for both comparisons (among Atlantic populations and among Baltic populations) or raw p<10−50 for a single comparison. These are the SNPs colored in red or black in Figure 3—figure supplement 3. Raw p-values are given in columns E and G and corrected p-values in columns F and H.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp5-v2.xlsx
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Supplementary file 6
Genes within inverted regions and 200 kb flanking inversion breakpoints on chromosome 6 and 17 in Atlantic herring.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp6-v2.xlsx
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Supplementary file 7
Reference allele frequencies for the 794 markers used in the PCA shown in Figure 2b.
- https://cdn.elifesciences.org/articles/61076/elife-61076-supp7-v2.xlsx
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Transparent reporting form
- https://cdn.elifesciences.org/articles/61076/elife-61076-transrepform-v2.docx
