Home LiteratureArticle Details
PMID: 21242529 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Evolution of modern birds revealed by mitogenomics: timing the radiation and origin of major orders.

Molecular biology and evolution ·Vol. 28 ·No. 6 ·2011-06-00 ·Pages 1927-42

Pacheco MA, Battistuzzi FU, Lentino M, Aguilar RF, Kumar S, Escalante AA

Abstract

Mitochondrial (mt) genes and genomes are among the major sources of data for evolutionary studies in birds. This places mitogenomic studies in birds at the core of intense debates in avian evolutionary biology. Indeed, complete mt genomes are actively been used to unveil the phylogenetic relationships among major orders, whereas single genes (e.g., cytochrome c oxidase I [COX1]) are considered standard for species identification and defining species boundaries (DNA barcoding). In this investigation, we study the time of origin and evolutionary relationships among Neoaves orders using complete mt genomes. First, we were able to solve polytomies previously observed at the deep nodes of the Neoaves phylogeny by analyzing 80 mt genomes, including 17 new sequences reported in this investigation. As an example, we found evidence indicating that columbiforms and charadriforms are sister groups. Overall, our analyses indicate that by improving the taxonomic sampling, complete mt genomes can solve the evolutionary relationships among major bird groups. Second, we used our phylogenetic hypotheses to estimate the time of origin of major avian orders as a way to test if their diversification took place prior to the Cretaceous/Tertiary (K/T) boundary. Such timetrees were estimated using several molecular dating approaches and conservative calibration points. Whereas we found time estimates slightly younger than those reported by others, most of the major orders originated prior to the K/T boundary. Finally, we used our timetrees to estimate the rate of evolution of each mt gene. We found great variation on the mutation rates among mt genes and within different bird groups. COX1 was the gene with less variation among Neoaves orders and the one with the least amount of rate heterogeneity across lineages. Such findings support the choice of COX 1 among mt genes as target for developing DNA barcoding approaches in birds.

MeSH Terms
Amino Acid Substitution/genetics Animals Birds/classification,genetics DNA, Mitochondrial/genetics Evolution, Molecular Genetic Variation Open Reading Frames/genetics Phylogeny
Chemicals
DNA, Mitochondrial
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Pacheco M Andreína
Center for Evolutionary Medicine and Informatics, The Biodesign Institute, Arizona State University, AZ, USA.
Battistuzzi Fabia U
Lentino Miguel
Aguilar Roberto F
Kumar Sudhir
Escalante Ananias A
References (66)
66 references, click to expand
  1. Phylogenetic relationships and divergence times of Charadriiformes genera: multigene evidence for the Cretaceous origin of at least 14 clades of shorebirds.
    Biol Lett. 2007 Apr 22;3(2):205-9 PMID: 17284401
  2. The rise of birds and mammals: are microevolutionary processes sufficient for macroevolution?
    Trends Ecol Evol. 2004 Oct;19(10):516-22 PMID: 16701316
  3. BEAST: Bayesian evolutionary analysis by sampling trees.
    BMC Evol Biol. 2007 Nov 08;7:214 PMID: 17996036
  4. Nuclear DNA does not reconcile 'rocks' and 'clocks' in Neoaves: a comment on Ericson et al.
    Biol Lett. 2007 Jun 22;3(3):257-9; discussion 260-1 PMID: 17389215
  5. Single mitochondrial gene barcodes reliably identify sister-species in diverse clades of birds.
    BMC Evol Biol. 2008 Mar 09;8:81 PMID: 18328107
  6. Resolving the root of the avian mitogenomic tree by breaking up long branches.
    Mol Phylogenet Evol. 2007 Jan;42(1):1-13 PMID: 16854605
  7. Definitive fossil evidence for the extant avian radiation in the Cretaceous.
    Nature. 2005 Jan 20;433(7023):305-8 PMID: 15662422
  8. Estimating sample sizes for DNA barcoding.
    Mol Phylogenet Evol. 2010 Mar;54(3):1035-9 PMID: 19761856
  9. Chromosomal analysis in Cathartidae: distribution of heterochromatic blocks and rDNA, and phylogenetic considerations.
    Genetica. 2009 Apr;135(3):299-304 PMID: 18504528
  10. The New Zealand biota: Historical background and new research.
    Trends Ecol Evol. 1993 Dec;8(12):429-33 PMID: 21236222
  11. Comment on "Hexapod origins: monophyletic or paraphyletic?".
    Science. 2003 Sep 12;301(5639):1482; author reply 1482 PMID: 12970547
  12. Mitochondrial and nuclear DNA sequences support a Cretaceous origin of Columbiformes and a dispersal-driven radiation in the Paleocene .
    Syst Biol. 2007 Aug;56(4):656-72 PMID: 17661233
  13. Use of mitogenomic information in teleostean molecular phylogenetics: a tree-based exploration under the maximum-parsimony optimality criterion.
    Mol Phylogenet Evol. 2000 Dec;17(3):437-55 PMID: 11133198
  14. A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the cretaceous.
    Mol Biol Evol. 2008 Oct;25(10):2141-56 PMID: 18653733
  15. RAG-1 sequences resolve phylogenetic relationships within Charadriiform birds.
    Mol Phylogenet Evol. 2003 Nov;29(2):268-78 PMID: 13678682
  16. The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals.
    BMC Evol Biol. 2009 Mar 10;9:54 PMID: 19284537
  17. Mammalian mitogenomic relationships and the root of the eutherian tree.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8151-6 PMID: 12034869
  18. Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates.
    Mol Biol Evol. 1996 Sep;13(7):933-42 PMID: 8752002
  19. The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes.
    Mol Biol Evol. 2000 Mar;17(3):451-7 PMID: 10723745
  20. Calibration of avian molecular clocks.
    Mol Biol Evol. 2001 Feb;18(2):206-13 PMID: 11158379
  21. A phylogenomic study of birds reveals their evolutionary history.
    Science. 2008 Jun 27;320(5884):1763-8 PMID: 18583609
  22. The root of the mammalian tree inferred from whole mitochondrial genomes.
    Mol Phylogenet Evol. 2003 Aug;28(2):171-85 PMID: 12878457
  23. Phylogenetic relationships and historical biogeography of neotropical parrots (Psittaciformes: Psittacidae: Arini) inferred from mitochondrial and nuclear DNA sequences.
    Syst Biol. 2006 Jun;55(3):454-70 PMID: 16861209
  24. Phylogenetic relationships within parrots (Psittacidae) inferred from mitochondrial cytochrome-b gene sequences.
    Zoolog Sci. 2006 Feb;23(2):191-8 PMID: 16603811
  25. Whole-genome phylogeny of mammals: evolutionary information in genic and nongenic regions.
    Proc Natl Acad Sci U S A. 2009 Oct 6;106(40):17077-82 PMID: 19805074
  26. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds.
    Mol Biol Evol. 2006 Jan;23(1):212-26 PMID: 16177230
  27. PAML 4: phylogenetic analysis by maximum likelihood.
    Mol Biol Evol. 2007 Aug;24(8):1586-91 PMID: 17483113
  28. MRBAYES: Bayesian inference of phylogenetic trees.
    Bioinformatics. 2001 Aug;17(8):754-5 PMID: 11524383
  29. Convergence and divergence in the evolution of aquatic birds.
    Proc Biol Sci. 2001 Jul 7;268(1474):1345-50 PMID: 11429133
  30. New candidate species most closely related to penguins.
    Gene. 2006 Aug 15;378:65-73 PMID: 16806742
  31. Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods.
    Mol Biol Evol. 2004 Feb;21(2):397-403 PMID: 14660685
  32. Multiple independent origins of mitochondrial gene order in birds.
    Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10693-7 PMID: 9724766
  33. A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock.
    Mol Biol Evol. 2006 Sep;23(9):1731-40 PMID: 16774978
  34. The evolution of the spindlin gene in birds: sequence analysis of an intron of the spindlin W and Z gene reveals four major divisions of the Psittaciformes.
    Mol Phylogenet Evol. 2005 Sep;36(3):706-21 PMID: 16099384
  35. More taxa, more characters: the hoatzin problem is still unresolved.
    Mol Biol Evol. 2003 Sep;20(9):1484-98 PMID: 12777516
  36. Divergence time and evolutionary rate estimation with multilocus data.
    Syst Biol. 2002 Oct;51(5):689-702 PMID: 12396584
  37. Bird evolution: testing the Metaves clade with six new mitochondrial genomes.
    BMC Evol Biol. 2008 Jan 23;8:20 PMID: 18215323
  38. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages.
    BMC Biol. 2008 Jan 28;6:6 PMID: 18226223
  39. Toward resolving deep neoaves phylogeny: data, signal enhancement, and priors.
    Mol Biol Evol. 2009 Feb;26(2):313-26 PMID: 18981298
  40. Explosive evolution in tertiary birds and mammals.
    Science. 1995 Feb 3;267(5198):637-8 PMID: 17745839
  41. Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event.
    Proc Biol Sci. 2001 Mar 7;268(1466):459-69 PMID: 11296857
  42. A genomic perspective on the shortcomings of mitochondrial DNA for "barcoding" identification.
    J Hered. 2006 Nov-Dec;97(6):581-94 PMID: 17135463
  43. Congruent avian phylogenies inferred from mitochondrial and nuclear DNA sequences.
    J Mol Evol. 2003 Jul;57(1):27-37 PMID: 12962303
  44. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion.
    Zool J Linn Soc. 2007 Jan 1;149(1):1-95 PMID: 18784798
  45. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
    Syst Biol. 2003 Oct;52(5):696-704 PMID: 14530136
  46. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
    Mol Biol Evol. 2007 Aug;24(8):1596-9 PMID: 17488738
  47. Combined mitochondrial and nuclear DNA sequences resolve the interrelations of the major Australasian marsupial radiations.
    Syst Biol. 2006 Feb;55(1):122-37 PMID: 16507529
  48. Evolution of craniofacial novelty in parrots through developmental modularity and heterochrony.
    Evol Dev. 2007 Nov-Dec;9(6):590-601 PMID: 17976055
  49. A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens.
    Proc Biol Sci. 2002 Feb 7;269(1488):235-41 PMID: 11839192
  50. Identification of Birds through DNA Barcodes.
    PLoS Biol. 2004 Oct;2(10):e312 PMID: 15455034
  51. Mass survival of birds across the Cretaceous-Tertiary boundary: molecular evidence.
    Science. 1997 Feb 21;275(5303):1109-13 PMID: 9027308
  52. Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution.
    Mol Biol Evol. 2006 Jun;23(6):1144-55 PMID: 16533822
  53. Site specific rates of mitochondrial genomes and the phylogeny of eutheria.
    BMC Evol Biol. 2007 Jan 25;7:8 PMID: 17254354
  54. Four new avian mitochondrial genomes help get to basic evolutionary questions in the late cretaceous.
    Mol Biol Evol. 2004 Jun;21(6):974-83 PMID: 14739240
  55. Europe's last Mesozoic bird.
    Naturwissenschaften. 2002 Sep;89(9):408-11 PMID: 12435093
  56. Flight of the dodo.
    Science. 2002 Mar 1;295(5560):1683 PMID: 11872833
  57. Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds.
    Proc Biol Sci. 2002 Apr 22;269(1493):839-46 PMID: 11958716
  58. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach.
    Mol Biol Evol. 2002 Jan;19(1):101-9 PMID: 11752195
  59. A molecular timescale for vertebrate evolution.
    Nature. 1998 Apr 30;392(6679):917-20 PMID: 9582070
  60. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative.
    Syst Biol. 2006 Aug;55(4):539-52 PMID: 16785212
  61. Inter-familial relationships of the shorebirds (Aves: Charadriiformes) based on nuclear DNA sequence data.
    BMC Evol Biol. 2003 Jul 23;3:16 PMID: 12875664
  62. Birds in a bush: five genes indicate explosive evolution of avian orders.
    Evolution. 2004 Feb;58(2):404-15 PMID: 15068356
  63. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.
    Syst Biol. 2010 May;59(3):307-21 PMID: 20525638
  64. Diversification of Neoaves: integration of molecular sequence data and fossils.
    Biol Lett. 2006 Dec 22;2(4):543-7 PMID: 17148284
  65. Mitochondrial genomes and avian phylogeny: complex characters and resolvability without explosive radiations.
    Mol Biol Evol. 2007 Jan;24(1):269-80 PMID: 17062634
  66. Performance of relaxed-clock methods in estimating evolutionary divergence times and their credibility intervals.
    Mol Biol Evol. 2010 Jun;27(6):1289-300 PMID: 20093431
Article Info
Journal
Molecular biology and evolution
Abbr.
Mol Biol Evol
ISSN
1537-1719
Published
2011-06-00
Epub
2011-00-17
Pages
1927-42
Language
English
Region
United States
NLM ID
8501455
PMCID
PMC3144022
Subset
IM
Grants
NIGMS NIH HHS · R01 GM080586 · United States
NIGMS NIH HHS · GM080586 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]