Letter

A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing

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Abstract

Although reconstruction of the phylogeny of living birds has progressed tremendously in the last decade, the evolutionary history of Neoaves—a clade that encompasses nearly all living bird species—remains the greatest unresolved challenge in dinosaur systematics. Here we investigate avian phylogeny with an unprecedented scale of data: >390,000 bases of genomic sequence data from each of 198 species of living birds, representing all major avian lineages, and two crocodilian outgroups. Sequence data were collected using anchored hybrid enrichment, yielding 259 nuclear loci with an average length of 1,523 bases for a total data set of over 7.8 × 107 bases. Bayesian and maximum likelihood analyses yielded highly supported and nearly identical phylogenetic trees for all major avian lineages. Five major clades form successive sister groups to the rest of Neoaves: (1) a clade including nightjars, other caprimulgiforms, swifts, and hummingbirds; (2) a clade uniting cuckoos, bustards, and turacos with pigeons, mesites, and sandgrouse; (3) cranes and their relatives; (4) a comprehensive waterbird clade, including all diving, wading, and shorebirds; and (5) a comprehensive landbird clade with the enigmatic hoatzin (Opisthocomus hoazin) as the sister group to the rest. Neither of the two main, recently proposed Neoavian clades—Columbea and Passerea1—were supported as monophyletic. The results of our divergence time analyses are congruent with the palaeontological record, supporting a major radiation of crown birds in the wake of the Cretaceous–Palaeogene (K–Pg) mass extinction.

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Change history

  • Updated online 12 October 2015

    The Supplementary Table 1 file was uploaded on 12 October 2015 as it was omitted at the time of online publication.

  • Updated online 27 October 2015

    The PDF was replaced with a higher-resolution version on October 27.

References

  1. 1.

    et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014)

  2. 2.

    & IOC World Bird List (v5.1) (2015)

  3. 3.

    Ornithology 2nd edn (W. H. Freeman and Co., 1995)

  4. 4.

    et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)

  5. 5.

    et al. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol. Lett. 2, 543–547 (2006)

  6. 6.

    et al. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS ONE 8, e54848 (2013)

  7. 7.

    Paleogene Fossil Birds (Springer, 2009)

  8. 8.

    Metaves, Mirandornithes, Strisores and other novelties — a critical review of the higher-level phylogeny of neornithine birds. J. Zoological Syst. Evol. Res. 49, 58–76 (2011)

  9. 9.

    Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47, 9–17 (1998)

  10. 10.

    , & Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46, 239–257 (2008)

  11. 11.

    & Optimal selection of gene and ingroup taxon sampling for resolving phylogenetic relationships. Syst. Biol. 59, 446–457 (2010)

  12. 12.

    , & Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst. Biol. 61, 727–744 (2012)

  13. 13.

    , , & PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701 (2012)

  14. 14.

    & A comprehensive multilocus phylogeny of the neotropical cotingas (Cotingidae, Aves) with a comparative evolutionary analysis of breeding system and plumage dimorphism and a revised phylogenetic classification. Mol. Phylogenet. Evol. 81, 120–136 (2014)

  15. 15.

    Profiling phylogenetic informativeness. Syst. Biol. 56, 222–231 (2007)

  16. 16.

    , & Phylogenetic signal and noise: predicting the power of a data set to resolve phylogeny. Syst. Biol. 61, 835–849 (2012)

  17. 17.

    , & ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31, 2553–2556 (2014)

  18. 18.

    RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014)

  19. 19.

    , , & Estimating species phylogenies using coalescence times among sequences. Syst. Biol. 58, 468–477 (2009)

  20. 20.

    & Estimating species trees from unrooted gene trees. Syst. Biol. 60, 661–667 (2011)

  21. 21.

    et al. ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30, i541–i548 (2014)

  22. 22.

    , , , & Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated conditions. PLOS Currents Tree of Life 1 (2015)

  23. 23.

    , & Evaluating summary methods for multi-locus species tree estimation in the presence of incomplete lineage sorting. Syst. Biol. (2014)

  24. 24.

    , , , & Phylogeny and diversification of the largest avian radiation. Proc. Natl Acad. Sci. USA 101, 11040–11045 (2004)

  25. 25.

    et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012)

  26. 26.

    , & Mass extinction of birds at the Cretaceous–Paleogene (K–Pg) boundary. Proc. Natl Acad. Sci. USA 108, 15253–15257 (2011)

  27. 27.

    The Origin and Evolution of Birds 2nd edn (Yale Univ. Press, 1999)

  28. 28.

    , , , & The global diversity of birds in space and time. Nature 491, 444–448 (2012)

  29. 29.

    Hummingbirds see near ultraviolet light. Science 207, 786–788 (1980)

  30. 30.

    , , , & Handbook of the Birds of the World Alive (Lynx Edicions, 2015)

  31. 31.

    & MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)

  32. 32.

    & Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. (2010)

  33. 33.

    , , & The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics 13, 312 (2012)

  34. 34.

    et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014)

  35. 35.

    , & The influence of model averaging on clade posteriors: an example using the triggerfishes (Family Balistidae). Syst. Biol. 57, 905–919 (2008)

  36. 36.

    Tracer. v1.6. (2014)

  37. 37.

    & in Combinatorial Mathematics VI in Lecture Notes in Mathematics, Vol. 748 (eds & ) Ch. 12 119–126 (Springer, 1979)

  38. 38.

    , & TreeCmp: comparison of trees in polynomial time. Evol. Bioinform. 8, 475–487 (2012)

  39. 39.

    Trees of Trees: an approach to comparing multiple alternative phylogenies. Syst. Biol. 57, 785–794 (2008)

  40. 40.

    phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011)

  41. 41.

    , , , & KDETREES: non-parametric estimation of phylogenetic tree distributions. Bioinformatics 30, 2280–2287 (2014)

  42. 42.

    , , & Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012)

  43. 43.

    & Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656 (2003)

  44. 44.

    , , & STRAW: species tree analysis web server. Nucleic Acids Res. 41, W238–W241 (2013)

  45. 45.

    , & A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evol. Biol. 10, 302 (2010)

  46. 46.

    & The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987)

  47. 47.

    , , & Statistical binning enables an accurate coalescent-based estimation of the avian tree. Science 346, (2014)

  48. 48.

    , & Evaluating summary methods for multilocus species tree estimation in the presence of incomplete lineage sorting. Syst. Biol. (2014)

  49. 49.

    & Naive binning improves phylogenomic analyses. Bioinformatics 29, 2277–2284 (2013)

  50. 50.

    & Fast and consistent estimation of species trees using supermatrix rooted triples. Mol. Biol. Evol. 27, 552–569 (2010)

  51. 51.

    , , , & Identifying localized biases in large datasets: a case study using the avian tree of life. Mol. Phylogenet. Evol. 69, 1021–1032 (2013)

  52. 52.

    et al. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS ONE 8, e54848 (2013)

  53. 53.

    & Land plant origins and coalescence confusion. Trends Plant Sci. 19, 267–269 (2014)

  54. 54.

    , , , & Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated conditions. PLOS Currents Tree of Life 1, (2015)

  55. 55.

    & in Statistical Methods in Molecular Evolution (ed. ) 125–181 (Springer, 2005)

  56. 56.

    & PhyDesign: an online application for profiling phylogenetic informativeness. BMC Evol. Biol. 11, 152 (2011)

  57. 57.

    A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14, 1218 (1997)

  58. 58.

    , & Relative character-state space, amount of potential phylogenetic information, and heterogeneity of nucleotide and amino acid characters. Mol. Phylogenet. Evol. 32, 913–926 (2004)

  59. 59.

    & Taxon sampling and the optimal rates of evolution for phylogenetic inference. Syst. Biol. 60, 358–365 (2011)

  60. 60.

    , & An evaluation of phylogenetic informativeness profiles and the molecular phylogeny of Diplazontinae (Hymenoptera, Ichneumonidae). Syst. Biol. 59, 226–241 (2010)

  61. 61.

    & Bayesian Evolutionary Analysis With BEAST (Cambridge Univ. Press, 2015)

  62. 62.

    et al. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evol. Biol. 15, 87 (2015)

  63. 63.

    , , & Tinamous and moa flock together: mitochondrial genome sequence analysis reveals independent losses of flight among ratites. Syst. Biol. 59, 90–107 (2010)

  64. 64.

    & A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock. Mol. Biol. Evol. 23, 1731–1740 (2006)

  65. 65.

    et al. Molecular evolution of genes in avian genomes. Genome Biol. 11, R68 (2010)

  66. 66.

    , , & Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006)

  67. 67.

    , et al. Relaxed clocks and inferences of heterogeneous patterns of nucleotide substitution and divergence time estimates across whales and dolphins (Mammalia: Cetacea). Mol. Biol. Evol. 29, 721–736 (2012)

  68. 68.

    & Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006)

  69. 69.

    Calibrating molecular estimates of substitution rates and divergence times in birds. J. Avian Biol. 38, 409–414 (2007)

  70. 70.

    & Calibrated tree priors for relaxed phylogenetics and divergence time estimation. Syst. Biol. 61, 138–149 (2012)

  71. 71.

    & Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26 (2007)

  72. 72.

    Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bull. Am. Mus. Nat. Hist. 286, 1–179 (2004)

  73. 73.

    , , & Pelagic neonatal fossils support viviparity and precocial life history of Cretaceous mosasaurs. Palaeontology 58, 401–407 (2015)

  74. 74.

    The age of the crown group of passerine birds and its evolutionary significance — molecular calibrations versus the fossil record. Syst. Biodivers. 11, 7–13 (2013)

  75. 75.

    et al. Global distribution and conservation of evolutionary distinctness in birds. Curr. Biol. 24, 919–930 (2014)

  76. 76.

    , , & Continental breakup and the ordinal diversification of birds and mammals. Nature 381, 226–229 (1996)

  77. 77.

    Early origins of modern birds and mammals: molecules vs. morphology. Bioessays 21, 1043–1051 (1999)

  78. 78.

    in Mesozoic Birds: Above the Heads of Dinosaurs (eds & ) 339–388 (Univ. of California Press, 2002)

  79. 79.

    , & Mass extinction of birds at the Cretaceous–Paleogene (K–Pg) boundary. Proc. Natl Acad. Sci. USA 108, 15253–15257 (2011)

  80. 80.

    , & Phylogenetic relationships and divergence times of Charadriiformes genera: multigene evidence for the Cretaceous origin of at least 14 clades of shorebirds. Biol. Lett. 3, 205–209 (2007)

  81. 81.

    et al. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. B 279, 3491–3500 (2012)

  82. 82.

    , , & Phylogenetic informativeness reconciles ray-finned fish molecular divergence times. BMC Evol. Biol. 14, 169 (2014)

  83. 83.

    et al. Accommodating heterogenous rates of evolution in molecular divergence dating methods: an example using intercontinental dispersal of Plestiodon (Eumeces) lizards. Syst. Biol. 60, 3–15 (2011)

  84. 84.

    Branch-length estimation bias misleads molecular dating for a vertebrate mitochondrial phylogeny. Gene 441, 132–140 (2009)

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Acknowledgements

The research was supported by W. R. Coe Funds from Yale University to R.O.P., and by NSF grants to A.R.L. and E.M.L. We thank the ornithology curators and staff of the following collections for granting research access to the invaluable avian tissue collections that made this work possible: American Museum of Natural History, Field Museum of Natural History, Royal Ontario Museum, University of Kansas Museum of Natural History and Biodiversity Research Center, University of Washington Burke Museum of Natural History, and Yale Peabody Museum of Natural History. We thank M. Kortyna and H. Ralicki for contributions to laboratory work, S. Gullapalli for computational assistance, and N. J. Carriero and R. D. Bjornson at the Yale University Biomedical High Performance Computing Center, which is supported by the NIH. Bird illustrations reproduced with permission from the Handbook of the Birds of the World Alive Online, Lynx Edicions, Barcelona30. The research was aided by discussions with R. Bowie, S. Edwards, I. Lovette, J. Musser, T. Near, and K. Zyskowski.

Author information

Author notes

    • Richard O. Prum
    •  & Jacob S. Berv

    These authors contributed equally to this work.

Affiliations

  1. Department of Ecology & Evolutionary Biology, Yale University, New Haven, Connecticut 06520, USA

    • Richard O. Prum
    • , Alex Dornburg
    •  & Jeffrey P. Townsend
  2. Peabody Museum of Natural History, Yale University, New Haven, Connecticut 06520, USA

    • Richard O. Prum
    • , Alex Dornburg
    •  & Daniel J. Field
  3. Department of Ecology and Evolutionary Biology, Fuller Evolutionary Biology Program, Cornell University, and Cornell Laboratory of Ornithology, Ithaca, New York 14853, USA

    • Jacob S. Berv
  4. North Carolina Museum of Natural Sciences, Raleigh, North Carolina 27601, USA

    • Alex Dornburg
  5. Department of Geology & Geophysics, Yale University, New Haven, Connecticut 06520, USA

    • Daniel J. Field
  6. Department of Biostatistics, and Program in Computational Biology and Bioinformatics, Yale University, NewHaven, Connecticut 06520, USA

    • Jeffrey P. Townsend
  7. Department of Biological Science, Florida State University, Tallahassee, Florida 32306, USA

    • Emily Moriarty Lemmon
  8. Department of Scientific Computing, Florida State University, Tallahassee, Florida 32306, USA

    • Alan R. Lemmon

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Contributions

R.O.P., J.S.B., A.R.L., and E.M.L. conceived of and designed the study. R.O.P. selected the taxa studied. A.R.L. selected the loci and designed the probes. J.S.B., A.R.L., and E.M.L. collected the data. J.S.B. and A.R.L. performed the phylogenetic analyses. A.D. and J.P.T. performed the phylogenetic informativeness, and signal and noise analyses. D.J.F. selected fossil taxa for calibration, and J.S.B., D.J.F., and A.D. designed and performed the dating analyses. R.O.P. wrote the paper with contributions from all other authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Richard O. Prum or Jacob S. Berv.

Electronic data files and software are permanently archived at http://dx.doi.org/10.5281/zenodo.28343.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and Data, Supplementary References and Supplementary Figures 1-12.

  2. 2.

    Supplementary Data

    This file contains Supplementary Table 1. This file was uploaded on 12 October 2015 as it was omitted at the time of online publication.

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