Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Ecology & Evolution volume 2, pages 1128–1138 (2018)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000).

  2. Grant, P. R. Speciation and the adaptive radiation of Darwin finches. Am. Sci. 69, 653–663 (1981).

    Google Scholar 

  3. Losos, J. B., Jackman, T. R., Larson, A., Queiroz, K. & Rodriguez-Schettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998).

    Article  CAS  PubMed  Google Scholar 

  4. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, Oxford, 2003).

  5. Muschick, M., Barluenga, M., Salzburger, W. & Meyer, A. Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol. Biol. 11, 116 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Barrett, R. D. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).

    Article  PubMed  Google Scholar 

  7. Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).

    Article  PubMed  Google Scholar 

  9. Meier, J. I. et al. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8, 14363 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Price, T. D., Qvarnstrom, A. & Irwin, D. E. The role of phenotypic plasticity in driving genetic evolution. Proc. Biol. Sci. 270, 1433–1440 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Schlotterer, C., Kofler, R., Versace, E., Tobler, R. & Franssen, S. U. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity (Edinb.) 116, 248 (2016).

    Article  CAS  Google Scholar 

  12. Barrett, S. C. H., Colautti, R. I., Dlugosch, K. M. & Rieseberg, L. H. Invasion Genetics: The Baker and Stebbins Legacy (Wiley-Blackwell, Hoboken, NJ, 2016).

  13. Burke, M. K. et al. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587–590 (2010).

    Article  CAS  PubMed  Google Scholar 

  14. Fritz, M. L. et al. Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices. Mol. Ecol. 27, 167–181 (2018).

    Article  PubMed  Google Scholar 

  15. Tobler, R. et al. Massive habitat-specific genomic response in D. melanogaster populations during experimental evolution in hot and cold environments. Mol. Biol. Evol. 31, 364–375 (2014).

    Article  CAS  PubMed  Google Scholar 

  16. Graves, J. L. et al. Genomics of parallel experimental evolution in Drosophila. Mol. Biol. Evol. 34, 831–842 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Huang, Y., Wright, S. I. & Agrawal, A. F. Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet. 10, e1004527 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Franks, S. J., Kane, N. C., O’Hara, N. B., Tittes, S. & Rest, J. S. Rapid genome-wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools. Mol. Ecol. 25, 3622–3631 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. van’t Hof, A. E., Edmonds, N., Dalikova, M., Marec, F. & Saccheri, I. J. Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332, 958–960 (2011).

    Article  PubMed  CAS  Google Scholar 

  20. Reid, N. M. et al. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354, 1305–1308 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fraser, B. A., Kunstner, A., Reznick, D. N., Dreyer, C. & Weigel, D. Population genomics of natural and experimental populations of guppies (Poecilia reticulata). Mol. Ecol. 24, 389–408 (2015).

    Article  PubMed  Google Scholar 

  22. Hendry, A. P. & Kinnison, M. T. Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53, 1637–1653 (1999).

    Article  PubMed  Google Scholar 

  23. Reznick, D. N. & Ghalambor, C. K. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112-113, 183–198 (2001).

    Article  CAS  PubMed  Google Scholar 

  24. Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 18, 94–101 (2003).

    Article  Google Scholar 

  25. Bell, M. A., Aguirre, W. E. & Buck, N. J. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58, 814–824 (2004).

    Article  PubMed  Google Scholar 

  26. Terekhanova, N. V. et al. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 10, e1004696 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Lescak, E. A. et al. Evolution of stickleback in 50 years on earthquake-uplifted islands. Proc. Natl Acad. Sci. USA 112, E7204–E7212 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Aguirre, W. E. & Bell, M. A. Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol. J. Linn. Soc. 105, 817–831 (2012).

    Article  Google Scholar 

  29. Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Reimchen, T. E., Bergstrom, C. & Nosil, P. Natural selection and the adaptive radiation of Haida Gwaii stickleback. Evol. Ecol. Res. 15, 241–269 (2013).

    Google Scholar 

  31. Moodie, G. E. E. & Reimchen, T. E. Phenetic variation and habitat differences in Gasterosteus populations of the Queen Charlotte Islands. Syst. Zool. 25, 49–61 (1976).

    Article  Google Scholar 

  32. Reimchen, T. E. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 240–276 (Oxford Univ. Press, Oxford, 1994).

  33. Bergstrom, C. A. & Reimchen, T. E. Habitat dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations. J. Evol. Biol. 18, 939–948 (2005).

    Article  CAS  PubMed  Google Scholar 

  34. Deagle, B. E., Jones, F. C., Absher, D. M., Kingsley, D. M. & Reimchen, T. E. Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide single nucleotide polymorphism genotyping. Mol. Ecol. 22, 1917–1932 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Reimchen, T. E. Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: functional implications for the ancestral plate condition. Behaviour 137, 1081–1096 (2000).

    Article  Google Scholar 

  36. Reimchen, T. E. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus—an adaptation to predators. Can. J. Zool. 58, 1232–1244 (1980).

    Article  Google Scholar 

  37. Reimchen, T. E. & Nosil, P. Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56, 2472–2483 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Reimchen, T. E. & Nosil, P. Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58, 1274–1281 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. Reimchen, T. E., Stinson, E. M. & Nelson, J. S. Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands. Can. J. Zool. 63, 2944–2951 (1985).

    Article  Google Scholar 

  40. Spoljaric, M. A. & Reimchen, T. E. 10 000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J. Fish. Biol. 70, 1484–1503 (2007).

    Article  Google Scholar 

  41. Leaver, S. D. & Reimchen, T. E. Abrupt changes in defence and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol. J. Linn. Soc. 107, 494–509 (2012).

    Article  Google Scholar 

  42. Moodie, G. E. E. Morphology, life-history, and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada. Can. J. Zool. 50, 721–732 (1972).

    Article  Google Scholar 

  43. Moodie, G. E. E. Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28, 155–167 (1972).

    Article  Google Scholar 

  44. Oreilly, P., Reimchen, T. E., Beech, R. & Strobeck, C. Mitochondrial DNA in Gasterosteus and pleistocene glacial refugium on the Queen Charlotte Islands, British Columbia. Evolution 47, 678–684 (1993).

    Article  CAS  Google Scholar 

  45. Flamarique, I. N., Bergstrom, C., Cheng, C. L. & Reimchen, T. E. Role of the iridescent eye in stickleback female mate choice. J. Exp. Biol. 216, 2806–2812 (2013).

    PubMed  Google Scholar 

  46. Deagle, B. E. et al. Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions. Proc. Biol. Sci. 279, 1277–1286 (2012).

    CAS  PubMed  Google Scholar 

  47. Peichel, C. L. & Marques, D. A. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Phil. Trans. R. Soc. Lond. B 372, 20150486 (2017).

    Article  Google Scholar 

  48. Peichel, C. L. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001).

    Article  CAS  PubMed  Google Scholar 

  49. Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).

    Article  CAS  PubMed  Google Scholar 

  50. Colosimo, P. F. et al. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2, E109 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wark, A. R. et al. Genetic architecture of variation in the lateral line sensory system of threespine sticklebacks. G3 2, 1047–1056 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Greenwood, A. K., Wark, A. R., Yoshida, K. & Peichel, C. L. Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr. Biol. 23, 1884–1888 (2013).

    Article  CAS  PubMed  Google Scholar 

  53. Rennison, D. J., Owens, G. L., Heckman, N., Schluter, D. & Veen, T. Rapid adaptive evolution of colour vision in the threespine stickleback radiation. Proc. Biol. Sci. 283, 20160242 (2016).

    PubMed  PubMed Central  Google Scholar 

  54. Perez-Leighton, C. E., Schmidt, T. M., Abramowitz, J., Birnbaumer, L. & Kofuji, P. Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur. J. Neurosci. 33, 856–867 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Nakajima, Y., Moriyama, M., Hattori, M., Minato, N. & Nakanishi, S. Isolation of ON bipolar cell genes via hrGFP-coupled cell enrichment using the mGluR6 promoter. J. Biochem. 145, 811–818 (2009).

    Article  CAS  PubMed  Google Scholar 

  56. Amsterdam, A. et al. Identification of 315 genes essential for early zebrafish development. Proc. Natl Acad. Sci. USA 101, 12792–12797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nuckels, R. J., Ng, A., Darland, T. & Gross, J. M. The vacuolar-ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Invest. Ophthalmol. Vis. Sci. 50, 893–905 (2009).

    Article  PubMed  Google Scholar 

  58. Howe, D. G. et al. ZFIN, the zebrafish model organism database: increased support for mutants and transgenics. Nucleic Acids Res. 41, D854–D860 (2013).

    Article  CAS  PubMed  Google Scholar 

  59. Marques, D. A. et al. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLoS Biol. 15, e2001627 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Gwynn, B., Smith, R. S., Rowe, L. B., Taylor, B. A. & Peters, L. L. A mouse TRAPP-related protein is involved in pigmentation. Genomics 88, 196–203 (2006).

    Article  CAS  PubMed  Google Scholar 

  61. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101–104 (2006).

    Article  CAS  PubMed  Google Scholar 

  62. Dickinson, M. E. et al. High-throughput discovery of novel developmental phenotypes. Nature 537, 508–514 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ignatius, M. S., Moose, H. E., El-Hodiri, H. M. & Henion, P. D. colgate/hdac1 repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev. Biol. 313, 568–583 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Patterson, L. B. & Parichy, D. M. Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet. 9, e1003561 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Miller, C. T. et al. cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131, 1179–1189 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Rosenblum, E. B., Hoekstra, H. E. & Nachman, M. W. Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution 58, 1794–1808 (2004).

    CAS  PubMed  Google Scholar 

  67. Malek, T. B., Boughman, J. W., Dworkin, I. & Peichel, C. L. Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback. Mol. Ecol. 21, 5265–5279 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Miller, C. T. et al. Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197, 405–420 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Lamichhaney, S. et al. A beak size locus in Darwin’s finches facilitated character displacement during a drought. Science 352, 470–474 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Gingerich, P. D. Rates of evolution: effects of time and temporal scaling. Science 222, 159–161 (1983).

    Article  CAS  PubMed  Google Scholar 

  71. Rennison, D. J., Owens, G. L. & Taylor, J. S. Opsin gene duplication and divergence in ray-finned fish. Mol. Phylogenet. Evol. 62, 986–1008 (2012).

    Article  PubMed  Google Scholar 

  72. Reimchen, T. E. Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus. Behaviour 132, 1079–1094 (1995).

    Article  Google Scholar 

  73. Stinson, E. M. Threespine Sticklebacks (Gasterosteus aculeatus) in Drizzle Lake and Its Inlet, Queen Charlotte Islands: Ecological and Behavioural Relationships and Their Relevance to Reproductive Isolation. MSc thesis, Univ. Alberta (1983).

  74. Dlugosch, K. M. & Parker, I. M. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431–449 (2008).

    Article  CAS  PubMed  Google Scholar 

  75. Keller, I. et al. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol. Ecol. 22, 2848–2863 (2013).

    Article  CAS  PubMed  Google Scholar 

  76. McGee, M. D., Neches, R. Y. & Seehausen, O. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25, 260–268 (2016).

    Article  CAS  PubMed  Google Scholar 

  77. Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).

    Article  CAS  PubMed  Google Scholar 

  78. Dasmahapatra, K. K. et al. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).

    Article  CAS  PubMed Central  Google Scholar 

  79. Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).

    Article  CAS  PubMed  Google Scholar 

  80. Glazer, A. M., Killingbeck, E. E., Mitros, T., Rokhsar, D. S. & Miller, C. T. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3 5, 1463–1472 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Delaneau, O., Howie, B., Cox, A. J., Zagury, J. F. & Marchini, J. Haplotype estimation using sequencing reads. Am. J. Hum. Genet. 93, 687–696 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y. & Wang, J. SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS ONE 7, e37558 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Fumagalli, M. et al. Quantifying population genetic differentiation from next-generation sequencing data. Genetics 195, 979–992 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  85. McLaren, W. et al. The Ensembl Variant Effect Predictor. Genome Biol. 17, 122 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Picard Tools (Broad Institute, 2017); http://broadinstitute.github.io/picard

  87. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strainw1118; iso-2; iso-3. Fly (Austin) 6, 80–92 (2012).

    Article  CAS  Google Scholar 

  88. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).

    Article  PubMed  Google Scholar 

  90. Willing, E. M., Dreyer, C. & van Oosterhout, C. Estimates of genetic differentiation measured by F ST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7, e42649 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Bhatia, G., Patterson, N., Sankararaman, S. & Price, A. L. Estimating and interpreting F ST: the impact of rare variants. Genome Res. 23, 1514–1521 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Excoffier, L., Dupanloup, I., Huerta-Sanchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Feulner, P. G. et al. Genomics of divergence along a continuum of parapatric population differentiation. PLoS Genet. 11, e1004966 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Garud, N. R., Messer, P. W., Buzbas, E. O. & Petrov, D. A. Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps. PLoS Genet. 11, e1005004 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, U913–U918 (2007).

    Article  CAS  Google Scholar 

  97. Szpiech, Z. A. & Hernandez, R. D. selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol. Biol. Evol. 31, 2824–2827 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016); http://www.r-project.org/

  99. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

    Google Scholar 

  100. Gillespie, J. H. Population Genetics: A Concise Guide 2nd edn (Johns Hopkins Univ. Press, Baltimore, MA, 2004).

  101. Szklarczyk, D. et al. STRINGv10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).

    Article  CAS  PubMed  Google Scholar 

  102. Blake, J. A. et al. Mouse Genome Database (MGD)-2017: community knowledge resource for the laboratory mouse. Nucleic Acids Res. 45, D723–D729 (2017).

    Article  CAS  PubMed  Google Scholar 

  103. Shimoyama, M. et al. The Rat Genome Database 2015: genomic, phenotypic and environmental variations and disease. Nucleic Acids Res. 43, D743–D750 (2015).

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Biology, University of Victoria, Victoria, British Columbia, Canada

    David A. Marques & Thomas E. Reimchen

  2. Aquatic Ecology & Evolution, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

    David A. Marques

  3. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland

    David A. Marques

  4. Department of Developmental Biology, HHMI and Stanford University School of Medicine, Stanford, CA, USA

    Felicity C. Jones & David M. Kingsley

  5. Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany

    Felicity C. Jones

  6. Earlham Institute, Norwich Research Park, Norwich, UK

    Federica Di Palma

  7. Department of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    Federica Di Palma

Authors
  1. David A. Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felicity C. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federica Di Palma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David M. Kingsley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas E. Reimchen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to David A. Marques.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Results, Supplementary Figures and Supplementary Data

Reporting Summary

Supplementary Tables

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0581-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing