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. Access through your institution Buy or subscribe This is

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ILLUMINATES THE DEVELOPMENTAL EVOLUTION OF RAY-FINNED FISHES Article Open access 30 August 2021 GENOMIC SIGNATURES OF CONVERGENT SHIFTS TO PLUNGE-DIVING BEHAVIOR IN BIRDS Article Open access

24 October 2023 A CHROMOSOME-LEVEL GENOME OF THE STRIATED FROGFISH (_ANTENNARIUS STRIATUS_) Article Open access 21 June 2024 ACCESSION CODES PRIMARY ACCESSIONS GENBANK/EMBL/DDBJ * KM891730

SEQUENCE READ ARCHIVE * PRJNA263122 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

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and the role of competition in macroevolution. _Ann. Rev. Evol. Ecol. Syst._ 44, 481–502 (2013) Article  Google Scholar  Download references 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 and Jonas Berglund: These authors contributed equally to this work. AUTHORS AND AFFILIATIONS * 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 * Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences,

SE-75007 Uppsala, Sweden, Khurram Maqbool & Leif Andersson * Department of Plant Physiology, Umeå University, SE-901 87 Umeå, Sweden, Neda Zamani * Department of Ecology and Evolutionary

Biology, Princeton University, Princeton, 08544, New Jersey, USA B. Rosemary Grant & Peter R. Grant * Department of Veterinary Integrative Biosciences, Texas A&M University, College

Station, 77843-4458, Texas, USA Leif Andersson Authors * Sangeet Lamichhaney View author publications You can also search for this author inPubMed Google Scholar * Jonas Berglund View

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Khurram Maqbool View author publications You can also search for this author inPubMed Google Scholar * Manfred Grabherr View author publications You can also search for this author inPubMed 

Google Scholar * Alvaro Martinez-Barrio View author publications You can also search for this author inPubMed Google Scholar * Marta Promerová View author publications You can also search

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also search for this author inPubMed Google Scholar * Neda Zamani View author publications You can also search for this author inPubMed Google Scholar * B. Rosemary Grant View author

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Scholar 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. 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) POWERPOINT SLIDES POWERPOINT SLIDE

FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 RIGHTS AND PERMISSIONS Reprints 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 Download citation * Received: 09

October 2014 * Accepted: 31 December 2014 * Published: 11 February 2015 * Issue Date: 19 February 2015 * DOI: https://doi.org/10.1038/nature14181 SHARE THIS ARTICLE Anyone you share the

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