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Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations

Abstract

Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides strong evidence of adaptation by natural selection. Many studies of parallelism focus on comparisons of different ecotypes or contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with components of environmental and phenotypic variation at an intercontinental scale across four freshwater adaptive radiations (Alaska, British Columbia, Iceland and Scotland) of the three-spined stickleback (Gasterosteus aculeatus). We combined large-scale biological sampling and phenotyping with restriction site associated DNA sequencing (RAD-Seq) data from 73 freshwater lake populations and four marine ones (1,380 fish) to associate genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. Our three main findings demonstrate that (1) quantitative variation in phenotypes and environments can predict genomic parallelism; (2) genomic parallelism at the early stages of adaptive radiations, even at large geographic scales, is founded on standing variation; and (3) similar environments are a better predictor of genome-wide parallelism than similar phenotypes. Overall, this study validates the importance and predictive power of major phenotypic and environmental factors likely to influence the emergence of common patterns of genomic divergence, providing a clearer picture than analyses of dichotomous phenotypes and environments.

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Fig. 1: Sampling sites and the bootstrapped unrooted NJ tree for stickleback from 73 freshwater lake populations and 4 marine populations from four countries on two continents, based on 11,266 genetic markers for 1,380 individuals.
Fig. 2: Comparisons and analyses of environmental and phenotypic parallelism across adaptive radiations.
Fig. 3: Expected and observed counts of 50-kb windows containing an above 99% binomial expectation number of SNPs associated with M × F, environmental variables and phenotypic traits in at least two radiations.
Fig. 4: Associations between genome-wide M × F FST and environmental, phenotypic and genetic distance across all pairwise comparisons of 73 freshwater populations.

Data availability

BAM files of the aligned reads for each individual and corresponding sample information have been deposited in the European Nucleotide Archive database under the project PRJEB20851, with the sample accession numbers ERS1831811–ERS1833111 and run accession numbers ERR2055459–ERR2056759.

Code availability

The scripts used for all analyses are archived through Github/Zenodo (https://doi.org/10.5281/zenodo.4024117).

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Acknowledgements

We thank S. Robertson, R. Young, A. Rahman, B. Santos, S. Goodacre, P. Halldorsson, B. K. Kristjánsson, D. Schluter, K. Samuk, D. Rennison and S. Miller for help with the sampling and sampling permits. We thank A. Lowe and L. Dean for help with the DNA extractions; C. Wiench, A. Stahlke and S. Hendricks for help making the RAD libraries; and J. Brookfield for discussion of the probability calculations. This work was funded by a NERC grant (no. NE/J02239X/1 to A.D.C.M.), and further support was provided by NIH grant no. P30GM103324.

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I.S.M., A.D.C.M. and J.R.W. conceived the project, interpreted the data and wrote the manuscript. I.S.M., D.D. and A.D.C.M. performed the fieldwork. I.S.M., M.M. and D.D. generated the phenotypic data. I.S.M. and P.A.H. generated the RAD data, and J.R.W., I.S.M. and P.A.H. analysed it. P.A.H., M.A.B. and S.S. helped with the sampling and revised the manuscript.

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Correspondence to Isabel S. Magalhaes or James R. Whiting.

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Supplementary Notes 1 and 2, Methods, Figs. 1–8, Tables 1–14, captions for Supplementary Data 1–3 and references.

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Supplementary Data 1

All Bayenv2 associated windows for window sizes of 50 kb, 75 kb, 100 kb, 200 kb and 0.1 cM.

Supplementary Data 2

Genes located in Bayenv2 associated windows along with GO information from Biomart.

Supplementary Data 3

Summary table with details of each individual analysed.

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Magalhaes, I.S., Whiting, J.R., D’Agostino, D. et al. Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations. Nat Ecol Evol 5, 251–261 (2021). https://doi.org/10.1038/s41559-020-01341-8

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