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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
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
Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000)
Seehausen, O. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. B 273, 1987–1998 (2006)
Lack, D. Darwin’s Finches (Cambridge Univ. Press, 1947)
Grant, P. R. Ecology and Evolution of Darwin’s Finches (Princeton Univ. Press, 1999)
Grant, P. R. & Grant, B. R. How and Why Species Multiply. The Radiation of Darwin’s Finches (Princeton Univ. Press, 2008)
Petren, K., Grant, P. R., Grant, B. R. & Keller, L. F. Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol. Ecol. 14, 2943–2957 (2005)
Ali, J. R. & Aitchison, J. C. Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. J. Biogeogr. 41, 1227–1241 (2014)
Geist, D., Snell, H., Snell, H., Goddard, C. & Kurz, M. in The Galápagos: A Natural Laboratory for the Earth Sciences (eds Harpp K. S., Mittelstaedt E., d’Ozouville N., & Graham, D. ) 145–166 (American Geophysical Union, 2014)
Farrington, H. L., Lawson, L. P., Clark, C. M. & Petren, K. The evolutionary history of Darwin’s finches: speciation, gene flow, and introgression in a fragmented landscape. Evolution 68, 2932–2944 (2014)
Abzhanov, A., Protas, M., Grant, B. R., Grant, P. R. & Tabin, C. J. Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305, 1462–1465 (2004)
Abzhanov, A. et al. The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–567 (2006)
Mallarino, R. et al. Two developmental modules establish 3D beak-shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 198, 4057–4062 (2011)
Burns, K. J. et al. Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Mol. Phylogenet. Evol. 75, 41–77 (2014)
Zhang, G., Parker, P., Li, B., Li, H. & Wang, J. The genome of Darwin’s finch (Geospiza fortis). GigaScience, http://dx.doi.org/10.5524/100040 (3 August 2012)
Ellegren, H. The evolutionary genomics of birds. Annu. Rev. Ecol. Evol. Syst. 44, 239–259 (2013)
Balakrishnan, C. N. & Edwards, S. V. Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the zebra finch (Taeniopygia guttata). Genetics 181, 645–660 (2009)
Swarth, H. S. The avifauna of the Galapagos Islands. Occ. Pap. Calif. Acad. Sci. 18, 1–299 (1931)
Lack, D. The Galapagos finches (Geospizinae): a study in variation. Occ. Pap. Calif. Acad. Sci. 21, 1–159 (1945)
Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011)
Qvarnstrom, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009)
Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011)
Rivera-Perez, J. A., Wakamiya, M. & Behringer, R. R. Goosecoid acts cell autonomously in mesenchyme-derived tissues during craniofacial development. Development 126, 3811–3821 (1999)
Rowe, A., Richman, J. M. & Brickell, P. M. Retinoic acid treatment alters the distribution of retinoic acid receptor-β transcripts in the embryonic chick face. Development 111, 1007–1016 (1991)
Uz, E. 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)
Dee, C. T., Szymoniuk, C. R., Mills, P. E. D. & Takahashi, T. Defective neural crest migration revealed by a zebrafish model of Alx1-related frontonasal dysplasia. Hum. Mol. Genet. 22, 239–251 (2013)
Brugmann, S. A. 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)
Sommer, P., Napier, H. R., Hogan, B. L. & Kidson, S. H. Identification of Tgfβ1i4 as a downstream target of Foxc1. Dev. Growth Differ. 48, 297–308 (2006)
Wang, J. 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)
Kumar, P., Henikoff, S. & Ng, P. C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature Protocols 4, 1073–1081 (2009)
Grant, P. R. & Grant, B. R. 40 Years of Evolution. Darwin’s Finches on Daphne Major Island (Princeton Univ. Press, 2014)
Boag, P. T. Growth and allometry of external morphology in Darwin’s finches (Geospiza) on Isla Daphne Major, Galápagos. J. Zool. 204, 413–441 (1984)
The Heliconius Genome Consortium Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012)
Andersson, L. Molecular consequences of animal breeding. Curr. Opin. Genet. Dev. 23, 295–301 (2013)
Linnen, C. R. et al. Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339, 1312–1316 (2013)
Siepel, A. et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034–1050 (2005)
Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 18 (2012)
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009)
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010)
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet. 43, 491–498 (2011)
Van der Auwera, G. A. 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)
Browning, S. R. & Browning, B. L. 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)
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007)
Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010)
Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979)
Rands, C. et al. Insights into the evolution of Darwin’s finches from comparative analysis of the Geospiza magnirostris genome sequence. BMC Genomics 14, 95 (2013)
Weir, J. T. & Schluter, D. Calibrating the avian molecular clock. Mol. Ecol. 17, 2321–2328 (2008)
Watterson, G. A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975)
Grant, B. R. & Grant, P. R. Demography and the genetically effective sizes of two populations of Darwin’s finches. Ecology 73, 766–784 (1992)
Nei, M. in Molecular Evolutionary Genetics 276–279 (Columbia Univ. Press, 1987)
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011)
Vilella, A. J. et al. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327–335 (2009)
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004)
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009)
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014)
Cingolani, P. 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)
Grant, B. R., Grant, P. R. & Petren, K. The allopatric phase of speciation: the sharp-beaked ground finch (Geospiza difficilis) on the Galápagos islands. Biol. J. Linn. Soc. 69, 287–317 (2000)
Grant, P. R., Abbott, I., Schluter, D., Curry, R. L. & Abbott, L. K. Variation in the size and shape of Darwin’s finches. Biol. J. Linn. Soc. 25, 1–39 (1985)
Schluter, D. & Grant, P. R. Ecological correlates of morphological evolution in a Darwin’s finch, Geospiza difficilis. Evolution 38, 856–869 (1984)
Rabosky, D. Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Ann. Rev. Evol. Ecol. Syst. 44, 481–502 (2013)
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
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 Read depth.
Average read depth in all 120 samples of Darwin’s finches and outgroup species.
Extended Data Figure 2 Genetic diversity among Darwin’s finches.
Heat map illustrating the proportion of shared and fixed polymorphisms among Darwin’s finches and outgroup species.
Extended Data Figure 3 Network tree for the Darwin’s finches on the basis of all autosomal sites.
Taxa that showed deviations from classical taxonomy are underscored. Finch heads are reproduced from ref. 5. How and Why Species Multiply: The Radiation of Darwin's Finches by Peter R. Grant & B. Rosemary Grant. Copyright © 2008 Princeton University Press. Reprinted by permission.
Extended Data Figure 4 Taxonomy and rate of speciation.
a, Morphological variation among populations of ground finch (Geospiza) species, scandens, fuliginosa and three others, acutirostris, difficilis and septentrionalis, that were formerly classified as a single species (difficilis). Data are from refs 56, 57, and from ref. 58 for weights and measures of difficilis on Fernandina. b, Morphological variation among populations of G. scandens, conirostris, propinqua and magnirostris assessed by multiple discriminant function analysis in JMP version 9. In a discriminant function analysis of the measured variables, all populations were correctly identified to species (−2 log likelihood P = 0.02). Maximum discrimination was achieved by entering three variables in the sequence beak width, beak length and body size (weight or wing). Substituting beak depth for beak width gave the same result. No other variable entered significantly. Data are from ref. 57, except for scandens and magnirostris data from ref. 30. c, Species accumulation on a log scale as a function of time before the present, dating based on mtDNA. Species are expected to accumulate linearly according to a ‘birth–death’ process, eventually declining under a density- (diversity-) dependent mechanism59.
Extended Data Figure 5 Phylogenies for mtDNA and the sex chromosomes Z and W.
a, Tree based on mtDNA sequences. The dating of the nodes and their variances (in thousands of years) is based on the cytochrome b sequences using the fossil-calibrated divergence rate 2.1% per million years for birds46. This tree based on the full mtDNA sequences shows only minor differences compared with previously published trees based only on the cytochrome b sequence6,9. b, Maximum-likelihood trees based on all Z-linked sites; all nodes having full local support on the basis of the Shimodaira–Hasegawa test are marked by asterisks. c, Tree based on W sequences, only females. Taxa that showed deviations from classical taxonomy are underscored (applies to a–c).
Extended Data Figure 6 ABBA–BABA analysis and demographic history.
a, ABBA–BABA analysis of G. magnirostris, G. conirostris on Española and on Genovesa, and with L. noctis as outgroup. b, Comparison of C. olivacea, C. fusca, a pool of all non-warblers, and with L. noctis as outgroup. The number of informative sites supporting the different trees is indicated both as a percentage and as the actual number. The D statistic and corresponding Holm–Bonferroni-corrected P value are also given for testing the null hypothesis of symmetry in genetic relationships. Finch heads are reproduced from ref. 5. c, PSMC analysis21 of all species except the G. difficilis group. d, PSMC analysis of the G. difficilis group.
Extended Data Figure 7 Sequence conservation of ALX1.
Amino-acid alignment of the complete ALX1 sequence among different vertebrates. Amino-acid substitutions between ALX1 alleles associated with blunt and pointed beaks are highlighted. The homeobox domain is indicated.
Supplementary information
Supplementary Information
This file contains Supplementary Text and References. (PDF 275 kb)
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. (XLSX 79 kb)
Supplementary Table 2
This file contains details from ABBA-BABA analyses of Darwin’s finch populations. P-values are two-sided Holm-Bonferroni corrected. (XLSX 59 kb)
Rights and permissions
About this article
Cite this article
Lamichhaney, S., Berglund, J., Almén, M. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015). https://doi.org/10.1038/nature14181
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature14181
This article is cited by
-
Gene flow and an anomaly zone complicate phylogenomic inference in a rapidly radiated avian family (Prunellidae)
BMC Biology (2024)
-
Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring
BMC Genomics (2024)
-
Recent beak evolution in North American starlings after invasion
Scientific Reports (2024)
-
Odor-regulated oviposition behavior in an ecological specialist
Nature Communications (2023)
-
Molecular mechanisms of adaptive evolution in wild animals and plants
Science China Life Sciences (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.