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Evolution of Darwin’s finches and their beaks revealed by genome sequencing

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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Figure 1: Sample locations and phylogeny of Darwin’s finches.
Figure 2: Population history.
Figure 3: A major locus controlling beak shape.

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.

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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

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Authors

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

Correspondence to Leif Andersson.

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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 ac).

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.

Extended Data Table 1 Phenotypic description of Darwin’s finches
Extended Data Table 2 Summary of samples of Darwin’s finches and outgroup species

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)

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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

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