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Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation

Abstract

A substantial part of biodiversity is thought to have arisen from adaptive radiations in which one lineage rapidly diversified into multiple lineages specialized to many different niches. However, selection and drift reduce genetic variation during adaptation to new niches and may thus prevent or slow down further niche shifts. We tested whether rapid adaptation is still possible from a highly derived ecotype in the adaptive radiation of threespine stickleback on the Haida Gwaii archipelago, Western Canada. In a 19-year selection experiment, we let giant sticklebacks from a large blackwater lake evolve in a small clearwater pond without vertebrate predators. A total of 56 whole genomes from the experiment and 26 natural populations revealed that adaptive genomic change was rapid in many small genomic regions and encompassed 75% of the change between 12,000-year-old ecotypes. Genomic change was as fast as phenotypic change in defence and trophic morphology, and both were largely parallel between the short-term selection experiment and long-term natural adaptive radiation. Our results show that functionally relevant standing genetic variation can persist in derived radiation members, allowing adaptive radiations to unfold very rapidly.

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Fig. 1: Phenotypic and genomic change in the selection experiment.
Fig. 2: Extent of phenotypic and genomic evolution in the 19-year selection experiment compared with the ~12,000-year-old adaptive radiation.
Fig. 3: Genomic footprints of divergent selection are widespread across the genome.
Fig. 4: Local signatures of divergent selection in the genome.
Fig. 5: Outlier regions and overlapping QTL, candidate genes and genotype-environment and genotype-phenotype (GE/GP) associations across the adaptive radiation.

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Acknowledgements

We thank B. Deagle, S. D. Leaver, C. B. Lowe, S. D. Brady, J. Turner, K. Lindblad-Toh and the Broad Institute Genomics Platform for help with sequences, samples and morphometric analysis, and B. Moa for bioinformatics support. This work was funded by the National Research Council Canada grant NRC2354 to T.E.R. and National Institute of Health grants 3P50HG002568-09S1 ARRA and 3P50HG002568 to D.M.K.

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T.E.R. conceived the study, ran the experiment, collected fish and ecological data in the field, and acquired morphological data. D.M.K., F.C.J. and F.D.P. generated sequencing data and genotype calls. D.A.M. designed and performed all subsequent analyses and wrote the manuscript with contributions from all co-authors.

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Correspondence to David A. Marques.

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Supplementary Table 1: List of genomic outlier regions. Supplementary Table 2: List of QTL overlapping with outlier regions. Supplementary Table 3: List of candidate genes centred on selective sweep signatures in outlier regions. Supplementary Table 4: Genomic evolution in the 13 generation selection experiment and beyond.

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Marques, D.A., Jones, F.C., Di Palma, F. et al. Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation. Nat Ecol Evol 2, 1128–1138 (2018). https://doi.org/10.1038/s41559-018-0581-8

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