Skip to content
naulon

No retraction, correction or concern found when last checked on Oct 19, 2026.

A Phylogeny of Birds Based on Over 1,500 Loci Collected by Target Enrichment and High-Throughput Sequencing

John E. McCormack, Michael G. Harvey, Brant C. Faircloth and 3 more

PLoS ONE · 2013

doi:10.1371/journal.pone.0054848

Abstract

Evolutionary relationships among birds in Neoaves, the clade comprising the vast majority of avian diversity, have vexed systematists due to the ancient, rapid radiation of numerous lineages. We applied a new phylogenomic approach to resolve relationships in Neoaves using target enrichment (sequence capture) and high-throughput sequencing of ultraconserved elements (UCEs) in avian genomes. We collected sequence data from UCE loci for 32 members of Neoaves and one outgroup (chicken) and analyzed data sets that differed in their amount of missing data. An alignment of 1,541 loci that allowed missing data was 87% complete and resulted in a highly resolved phylogeny with broad agreement between the Bayesian and maximum-likelihood (ML) trees. Although results from the 100% complete matrix of 416 UCE loci were similar, the Bayesian and ML trees differed to a greater extent in this analysis, suggesting that increasing from 416 to 1,541 loci led to increased stability and resolution of the tree. Novel results of our study include surprisingly close relationships between phenotypically divergent bird families, such as tropicbirds (Phaethontidae) and the sunbittern (Eurypygidae) as well as between bustards (Otididae) and turacos (Musophagidae). This phylogeny bolsters support for monophyletic waterbird and landbird clades and also strongly supports controversial results from previous studies, including the sister relationship between passerines and parrots and the non-monophyly of raptorial birds in the hawk and falcon families. Although significant challenges remain to fully resolving some of the deep relationships in Neoaves, especially among lineages outside the waterbirds and landbirds, this study suggests that increased data will yield an increasingly resolved avian phylogeny.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

Read at PubMed Central

References 73

  1. 1.

    Feduccia A (1999) The origin and evolution of birds. New Haven, Connecticut: Yale University Press.

    Not in our library

  2. 2.

    Ericson PGP, Anderson CL, Britton T, Elzanowski A, Johansson US, et al (2006 ) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2: 543–547.

    Not in our library10.1098/rsbl.2006.0523

  3. 3.
  4. 4.

    Chojnowski JL, Kimball RT, Braun EL (2008 ) Introns outperform exons in analyses of basal avian phylogeny using clathrin heavy chain genes. Gene 410: 89–96.

    Not in our library10.1016/j.gene.2007.11.016

  5. 5.

    Cracraft J, Barker FK, Braun M, Harshman J, Dyke GJ, et al.. (2004) Phylogenetic relationships among modern birds (Neornithes): toward an avian tree of life. In: Cracraft J, Donoghue M, editors. Assembling the tree of life. New York, NY: Oxford University Press. 468–489.

    Not in our library

  6. 6.

    Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, et al (2008 ) A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763–1768.

    Not in our library10.1126/science.1157704

  7. 7.

    Wang N, Braun EL, Kimball RT (2012 ) Testing hypotheses about the sister group of the Passeriformes using an independent 30-locus data set. Mol Biol Evol 29: 737–750.

    Not in our library10.1093/molbev/msr230

  8. 8.

    Zink RM, Barrowclough GF (2008 ) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17: 2107–2121.

    Not in our library10.1111/j.1365-294x.2008.03737.x

  9. 9.

    Whitfield JB, Lockhart PJ (2007 ) Deciphering ancient rapid radiations. Trends Ecol Evol 22: 258–265.

    Not in our library10.1016/j.tree.2007.01.012

  10. 10.

    Rokas A, Holland PWH (2000 ) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15: 454–459.

    Not in our library10.1016/s0169-5347(00)01967-4

  11. 11.

    Shedlock AM, Takahashi K, Okada N (2004 ) SINEs of speciation: tracking lineages with retroposons. Trends Ecol Evol 19: 545–553.

    Not in our library10.1016/j.tree.2004.08.002

  12. 12.

    Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, et al (2011 ) Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nature Comm 2: 443.

    Not in our library10.1038/ncomms1448

  13. 13.

    Matzke A, Churakov G, Berkes P, Arms EM, Kelsey D, et al (2012 ) Retroposon insertion patterns of neoavian birds: strong evidence for an extensive incomplete lineage sorting era. Mol Biol Evol 29: 1497–1501.

    Not in our library10.1093/molbev/msr319

  14. 14.

    Han KL, Braun EL, Kimball RT, Reddy S, Bowie RCK, et al (2011 ) Are transposable element insertions homoplasy free?: an examination using the avian tree of life. Syst Biol 60: 375–386.

    Not in our library10.1093/sysbio/syq100

  15. 15.

    Maddison WP (1997 ) Gene trees in species trees. Syst Biol 46: 523–536.

    Not in our library

  16. 16.

    Degnan JH, Salter LA (2005 ) Gene tree distributions under the coalescent process. Evolution 59: 24–37.

    Not in our library

  17. 17.

    Avise JC, Robinson TJ (2008 ) Hemiplasy: a new term in the lexicon of phylogenetics. Syst Biol 57: 503–507.

    Not in our library10.1080/10635150802164587

  18. 18.

    Knowles L (2009 ) Estimating species trees: methods of phylogenetic analysis when there is incongruence across genes. Syst Biol 58: 463–467.

    Not in our library10.1093/sysbio/syp061

  19. 19.

    Edwards SV (2008 ) Is a new and general theory of molecular systematics emerging? Evolution 63: 1–19.

    Not in our library10.1111/j.1558-5646.2008.00549.x

  20. 20.

    Liu L, Yu L, Kubatko LS, Pearl DK, Edwards SV (2009 ) Coalescent methods for estimating phylogenetic trees. Mol Phylogenet Evol 53: 320–328.

    Not in our library10.1016/j.ympev.2009.05.033

  21. 21.

    Edwards SV, Jennings WB, Shedlock AM (2005 ) Phylogenetics of modern birds in the era of genomics. Proc R Soc B 272: 979.

    Not in our library10.1098/rspb.2004.3035

  22. 22.
  23. 23.

    Fain MG, Houde P (2004 ) Parallel radiations in the primary clades of birds. Evolution 58: 2558–2573.

    Not in our library10.1111/j.0014-3820.2004.tb00884.x

  24. 24.

    Groth JG, Barrowclough GF (1999 ) Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Mol Phylogenet Evol 12: 115–123.

    Not in our library10.1006/mpev.1998.0603

  25. 25.

    Haddrath O, Baker AJ (2012) Multiple nuclear genes and retroposons support vicariance and dispersal of the palaeognaths, and an Early Cretaceous origin of modern birds. Proc Roy Soc B In press.

    Not in our library10.1098/rspb.2012.1630

  26. 26.

    Gibb GC, Penny D (2010 ) Two aspects along the continuum of pigeon evolution: A South-Pacific radiation and the relationship of pigeons within Neoaves. Mol Phylogenet Evol 56: 698–706.

    Not in our library10.1016/j.ympev.2010.04.016

  27. 27.

    Pratt RC, Gibb GC, Morgan-Richards M, Phillips MJ, Hendy MD, et al (2009 ) Toward resolving deep Neoaves phylogeny: data, signal enhancement, and priors. Mol Biol Evol 26: 313–326.

    Not in our library10.1093/molbev/msn248

  28. 28.

    Pacheco MA, Battistuzzi FU, Lentino M, Aguilar RF, Kumar S, et al (2011 ) Evolution of modern birds revealed by mitogenomics: timing the radiation and origin of major orders. Mol Biol Evol 28: 1927–1942.

    Not in our library10.1093/molbev/msr014

  29. 29.
  30. 30.

    Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, et al (2004 ) Ultraconserved elements in the human genome. Science 304: 1321–1325.

    Not in our library10.1126/science.1098119

  31. 31.

    Janes DE, Chapus C, Gondo Y, Clayton DF, Sinha S, et al (2011 ) Reptiles and mammals have differentially retained long conserved noncoding sequences from the Amniote ancestor. Genome Biol Evol 3: 102–113.

    Not in our library10.1093/gbe/evq087

  32. 32.

    Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al (2005 ) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034–1050.

    Not in our library10.1101/gr.3715005

  33. 33.

    Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, et al (2012 ) Ultraconserved elements anchor thousands of genetic markers for target enrichment spanning multiple evolutionary timescales. Syst Biol 61: 717–726.

    Not in our library10.1093/sysbio/sys004

  34. 34.

    Crawford NG, Faircloth BC, McCormack JE, Brumfield RT, Winker K, et al (2012 ) More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol Lett 8: 783–786.

    Not in our library10.1098/rsbl.2012.0331

  35. 35.

    McCormack JE, Faircloth BC, Crawford NG, Gowaty PA, Brumfield RT, et al (2012 ) Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis. Genome Res 22: 746–754.

    Not in our library10.1101/gr.125864.111

  36. 36.

    Derti A, Roth FP, Church GM, Wu C-t (2006 ) Mammalian ultraconserved elements are strongly depleted among segmental duplications and copy number variants. Nat Genet 38: 1216–1220.

    Not in our library10.1038/ng1888

  37. 37.

    Sibley CG, Monroe BL (1990) Distribution and taxonomy of birds of the world. New Haven: Yale University Press.

    Not in our library

  38. 38.

    Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor: CSHL Press.

    Not in our library

  39. 39.
  40. 40.

    Zerbino DR, Birney E (2008 ) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

    Not in our library10.1101/gr.074492.107

  41. 41.
  42. 42.

    Ronquist F, Huelsenbeck JP (2003 ) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.

    Not in our library10.1093/bioinformatics/btg180

  43. 43.

    Rambaut A, Drummond AJ (2007) Tracer - MCMC Trace Analysis Tool, v1.4. Available from: <http://beastbioedacuk/Tracer/>.

    Not in our library

  44. 44.

    Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008 ) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581–583.

    Not in our library10.1093/bioinformatics/btm388

  45. 45.

    Stamatakis A (2006 ) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

    Not in our library10.1093/bioinformatics/btl446

  46. 46.

    Stamatakis A, Hoover P, Rougemont J (2008 ) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758–771.

    Not in our library10.1080/10635150802429642

  47. 47.

    Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al (2010 ) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.

    Not in our library10.1093/sysbio/syq010

  48. 48.

    Liu L, Yu L, Pearl DK, Edwards SV (2009 ) Estimating species phylogenies using coalescence times among sequences. Syst Biol 58: 468–477.

    Not in our library10.1093/sysbio/syp031

  49. 49.

    Seo TK (2008 ) Calculating bootstrap probabilities of phylogeny using multilocus sequence data. Mol Biol Evol 25: 960–971.

    Not in our library10.1093/molbev/msn043

  50. 50.

    Nabholz B, Kunstner A, Wang R, Jarvis ED, Ellegren H (2011 ) Dynamic evolution of base composition: causes and consequences in avian phylogenomics. Mol Biol Evol 28: 2197–2210.

    Not in our library10.1093/molbev/msr047

  51. 51.

    Wiens JJ, Tiu J (2012 ) Highly incomplete taxa can rescue phylogenetic analyses from the negative impacts of limited taxon sampling. PLoS One 7: e42925.

    Not in our library10.1371/journal.pone.0042925

  52. 52.

    Wiens JJ, Morrill MC (2011 ) Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Syst Biol 60: 719–731.

    Not in our library10.1093/sysbio/syr025

  53. 53.

    Edwards SV, Liu L, Pearl DK (2007 ) High-resolution species trees without concatenation. Proc Natl Acad Sci USA 104: 5936–5841.

    Not in our library10.1073/pnas.0607004104

  54. 54.

    Kubatko L, Degnan J (2007 ) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56: 17–24.

    Not in our library10.1080/10635150601146041

  55. 55.

    Mossel E, Vigoda E (2005 ) Phylogenetic MCMC algorithms are misleading on mixtures of trees. Science 309: 2207–2209.

    Not in our library10.1126/science.1115493

  56. 56.

    Suzuki Y, Glazko GV, Nei M (2002 ) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci USA 25: 16138–16143.

    Not in our library10.1073/pnas.212646199

  57. 57.

    Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJP (2003 ) Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol 20: 248–254.

    Not in our library10.1093/molbev/msg042

  58. 58.

    Kolaczkowski B, Thornton JW (2006 ) Is there a star tree paradox? Mol Biol Evol 23: 1819–1823.

    Not in our library10.1093/molbev/msl059

  59. 59.

    Lewis PO, Holder MT, Holsinger KE (2005 ) Polytomies and Bayesian phylogenetic inference. Syst Biol 54: 241–253.

    Not in our library10.1080/10635150590924208

  60. 60.
  61. 61.

    Erixon P, Svennblad B, Britton T, Oxelman B (2003 ) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Syst Biol 52: 665–673.

    Not in our library10.1080/10635150390235485

  62. 62.

    Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002 ) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51: 673–688.

    Not in our library10.1080/10635150290102366

  63. 63.

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

    Not in our library

  64. 64.

    Chubb AL (2004 ) New nuclear evidence for the oldest divergence among neognath birds: the phylogenetic utility of ZENK (i). Mol Phylogenet Evol 30: 140–151.

    Not in our library10.1016/s1055-7903(03)00159-3

  65. 65.

    van Tuinen M, Butvill DB, Kirsch JAW, Hedges SB (2001 ) Convergence and divergence in the evolution of aquatic birds. Proc R Soc Lond B 268: 1345–1350.

    Not in our library10.1098/rspb.2001.1679

  66. 66.
  67. 67.

    Sorenson MD, Oneal E, Garcia-Moreno J, Mindell DP (2003 ) More taxa, more characters: the hoatzin problem is still unresolved. Mol Biol Evol 20: 1484–1498.

    Not in our library10.1093/molbev/msg157

  68. 68.

    Thomas B (1996) Family Opisthocomidae (hoatzins). In: del Hoyo J, Jordi A, Sargatal C, editors. Handbook of the birds of the world, volume 3, hoatzins to auks. Barcelona: Lynx Ediciones. 24–32.

    Not in our library

  69. 69.

    Glenn TC, French JO, Heincelman TJ, Jones KL, Sawyer RH (2008 ) Evolutionary relationships among copies of feather beta (β) keratin genes from several avian orders. Integr Comp Biol 48: 463–475.

    Not in our library10.1093/icb/icn061

  70. 70.

    Pasko L, Ericson PGP, Elzanowski A (2011 ) Phylogenetic utility and evolution of indels: A study in neognathous birds. Mol Phylogenet Evol 61: 760–771.

    Not in our library10.1016/j.ympev.2011.07.021

  71. 71.

    Prychitko TM, Moore WS (2003 ) Alignment and phylogenetic analysis of β-fibrinogen intron 7 sequences among avian orders reveal conserved regions within the intron. Mol Biol Evol 20: 762–771.

    Not in our library10.1093/molbev/msg080

  72. 72.

    Poe S, Chubb AL (2004 ) Birds in a bush: five genes indicate explosive evolution of avian orders. Evolution 58: 404–415.

    Not in our library

  73. 73.

    Haussler D, O’Brien SJ, Ryder OA, Barker FK, Clamp M, et al (2009 ) Genome 10 K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species. J Hered 100: 659–674.

    Not in our library10.1093/jhered/esp086

Cited by papers we hold 13

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.