Abstract

Darwin’s finches, inhabiting the Galápagos archipelago and Cocos Island, constitute an iconic model for studies of speciation and adaptive evolution. Here we report the results of whole-genome re-sequencing of 120 individuals representing all of the Darwin’s finch species and two close relatives. Phylogenetic analysis reveals important discrepancies with the phenotype-based taxonomy. We find extensive evidence for interspecific gene flow throughout the radiation. Hybridization has given rise to species of mixed ancestry. A 240 kilobase haplotype encompassing the ALX1 gene that encodes a transcription factor affecting craniofacial development is strongly associated with beak shape diversity across Darwin's finch species as well as within the medium ground finch (Geospiza fortis), a species that has undergone rapid evolution of beak shape in response to environmental changes. The ALX1 haplotype has contributed to diversification of beak shapes among the Darwin’s finches and, thereby, to an expanded utilization of food resources.

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Accessions

Primary accessions

GenBank/EMBL/DDBJ

Sequence Read Archive

Data deposits

The Illumina reads have been submitted to the short reads archive (http://www.ncbi.nlm.nih.gov/sra) under accession number PRJNA263122 and the consensus sequence for the G. fortis mtDNA has been submitted to GenBank under accession number KM891730.

References

  1. 1.

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

  2. 2.

    African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. B 273, 1987–1998 (2006)

  3. 3.

    Darwin’s Finches (Cambridge Univ. Press, 1947)

  4. 4.

    Ecology and Evolution of Darwin’s Finches (Princeton Univ. Press, 1999)

  5. 5.

    & How and Why Species Multiply. The Radiation of Darwin’s Finches (Princeton Univ. Press, 2008)

  6. 6.

    , , & Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol. Ecol. 14, 2943–2957 (2005)

  7. 7.

    & Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. J. Biogeogr. 41, 1227–1241 (2014)

  8. 8.

    , , , & in The Galápagos: A Natural Laboratory for the Earth Sciences (eds , , , & ) 145–166 (American Geophysical Union, 2014)

  9. 9.

    , , & The evolutionary history of Darwin’s finches: speciation, gene flow, and introgression in a fragmented landscape. Evolution 68, 2932–2944 (2014)

  10. 10.

    , , , & Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305, 1462–1465 (2004)

  11. 11.

    et al. The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–567 (2006)

  12. 12.

    et al. Two developmental modules establish 3D beak-shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 198, 4057–4062 (2011)

  13. 13.

    et al. Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Mol. Phylogenet. Evol. 75, 41–77 (2014)

  14. 14.

    , , , & The genome of Darwin’s finch (Geospiza fortis). GigaScience, (3 August 2012)

  15. 15.

    The evolutionary genomics of birds. Annu. Rev. Ecol. Evol. Syst. 44, 239–259 (2013)

  16. 16.

    & Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the zebra finch (Taeniopygia guttata). Genetics 181, 645–660 (2009)

  17. 17.

    The avifauna of the Galapagos Islands. Occ. Pap. Calif. Acad. Sci. 18, 1–299 (1931)

  18. 18.

    The Galapagos finches (Geospizinae): a study in variation. Occ. Pap. Calif. Acad. Sci. 21, 1–159 (1945)

  19. 19.

    , , & Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011)

  20. 20.

    & Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009)

  21. 21.

    & Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011)

  22. 22.

    , & Goosecoid acts cell autonomously in mesenchyme-derived tissues during craniofacial development. Development 126, 3811–3821 (1999)

  23. 23.

    , & Retinoic acid treatment alters the distribution of retinoic acid receptor-β transcripts in the embryonic chick face. Development 111, 1007–1016 (1991)

  24. 24.

    et al. Disruption of ALX1 causes extreme microphthalmia and severe facial clefting: expanding the spectrum of autosomal-recessive ALX-related frontonasal dysplasia. Am. J. Hum. Genet. 86, 789–796 (2010)

  25. 25.

    , , & Defective neural crest migration revealed by a zebrafish model of Alx1-related frontonasal dysplasia. Hum. Mol. Genet. 22, 239–251 (2013)

  26. 26.

    et al. Comparative gene expression analysis of avian embryonic facial structures reveals new candidates for human craniofacial disorders. Hum. Mol. Genet. 19, 920–930 (2010)

  27. 27.

    , , & Identification of Tgfβ1i4 as a downstream target of Foxc1. Dev. Growth Differ. 48, 297–308 (2006)

  28. 28.

    et al. Factorbook.org: a Wiki-based database for transcription factor-binding data generated by the ENCODE consortium. Nucleic Acids Res. 41, D171–D176 (2013)

  29. 29.

    , & Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature Protocols 4, 1073–1081 (2009)

  30. 30.

    & 40 Years of Evolution. Darwin’s Finches on Daphne Major Island (Princeton Univ. Press, 2014)

  31. 31.

    Growth and allometry of external morphology in Darwin’s finches (Geospiza) on Isla Daphne Major, Galápagos. J. Zool. 204, 413–441 (1984)

  32. 32.

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

  33. 33.

    Molecular consequences of animal breeding. Curr. Opin. Genet. Dev. 23, 295–301 (2013)

  34. 34.

    et al. Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339, 1312–1316 (2013)

  35. 35.

    et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034–1050 (2005)

  36. 36.

    et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 18 (2012)

  37. 37.

    & Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009)

  38. 38.

    et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010)

  39. 39.

    et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet. 43, 491–498 (2011)

  40. 40.

    et al. From FastQ data to high-confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinform. 43, 11.10.1–11.10.33 (2002)

  41. 41.

    & Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084–1097 (2007)

  42. 42.

    et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007)

  43. 43.

    et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010)

  44. 44.

    A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979)

  45. 45.

    et al. Insights into the evolution of Darwin’s finches from comparative analysis of the Geospiza magnirostris genome sequence. BMC Genomics 14, 95 (2013)

  46. 46.

    & Calibrating the avian molecular clock. Mol. Ecol. 17, 2321–2328 (2008)

  47. 47.

    On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975)

  48. 48.

    & Demography and the genetically effective sizes of two populations of Darwin’s finches. Ecology 73, 766–784 (1992)

  49. 49.

    in Molecular Evolutionary Genetics 276–279 (Columbia Univ. Press, 1987)

  50. 50.

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

  51. 51.

    et al. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327–335 (2009)

  52. 52.

    MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004)

  53. 53.

    , , , & Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009)

  54. 54.

    et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014)

  55. 55.

    et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6, 80–92 (2012)

  56. 56.

    , & The allopatric phase of speciation: the sharp-beaked ground finch (Geospiza difficilis) on the Galápagos islands. Biol. J. Linn. Soc. 69, 287–317 (2000)

  57. 57.

    , , , & Variation in the size and shape of Darwin’s finches. Biol. J. Linn. Soc. 25, 1–39 (1985)

  58. 58.

    & Ecological correlates of morphological evolution in a Darwin’s finch, Geospiza difficilis. Evolution 38, 856–869 (1984)

  59. 59.

    Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Ann. Rev. Evol. Ecol. Syst. 44, 481–502 (2013)

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Acknowledgements

The National Science Foundation (USA) funded the collection of material under permits from the Galápagos and Costa Rica National Parks Services, and in accordance with protocols of Princeton University’s Animal Welfare Committee. The map and images of finch heads are reproduced with permission from Princeton University Press. The project was supported by the Knut and Alice Wallenberg Foundation. Sequencing was performed by the SNP&SEQ Technology Platform, supported by Uppsala University and Hospital, SciLifeLab and Swedish Research Council (80576801 and 70374401). Computer resources were supplied by UPPMAX.

Author information

Author notes

    • Sangeet Lamichhaney
    •  & Jonas Berglund

    These authors contributed equally to this work.

Affiliations

  1. Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden

    • Sangeet Lamichhaney
    • , Jonas Berglund
    • , Markus Sällman Almén
    • , Manfred Grabherr
    • , Alvaro Martinez-Barrio
    • , Marta Promerová
    • , Carl-Johan Rubin
    • , Chao Wang
    • , Neda Zamani
    • , Matthew T. Webster
    •  & Leif Andersson
  2. Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden

    • Khurram Maqbool
    •  & Leif Andersson
  3. Department of Plant Physiology, Umeå University, SE-901 87 Umeå, Sweden

    • Neda Zamani
  4. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA

    • B. Rosemary Grant
    •  & Peter R. Grant
  5. Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas 77843-4458, USA

    • Leif Andersson

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Contributions

P.R.G. and B.R.G. collected the material. L.A., P.R.G. and B.R.G. conceived the study. L.A. and M.T.W. led the bioinformatic analysis of data. S.L. and J.B. performed the bioinformatic analysis with contributions from M.S.A., K.M., M.G., A.M.-B., C.-J.R. and N.Z. M.P. and C.W. performed experimental work. L.A., S.L., J.B., B.R.G., P.R.G. and M.T.W. wrote the paper with input from the other authors. All authors approved the manuscript before submission.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Leif Andersson.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and References.

Excel files

  1. 1.

    Supplementary Table 1

    This file contains read depth in males and females for the identification of scaffolds from chromosome Z and W. Part a shows read depth in males and females for scaffolds assigned to the Z chromosome. Part b shows read depth in males and females for scaffolds assigned to the W chromosome.

  2. 2.

    Supplementary Table 2

    This file contains details from ABBA-BABA analyses of Darwin’s finch populations. P-values are two-sided Holm-Bonferroni corrected.

About this article

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DOI

https://doi.org/10.1038/nature14181

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