Alignment and phylogenetic analysis of beta-fibrinogen intron 7 sequences among avian orders reveal conserved regions within the intron.

We sequenced beta-fibrinogen intron 7 (beta-fibint 7) from 28 species of birds, representing 18 families in nine orders. Although the antiquity of the avian orders is estimated to be 55 to 90 Myr, and numerous indels have accrued among diverging lineages, the intron sequences were not difficult to align. However, alignment of avian sequences with mammal or snake sequences was difficult, and the residual phylogenetic signal was weak. beta-fibint 7 is an AT-rich intron, and its base composition varies little over the diversity of birds represented by our sample. Alignment of these anciently diverged sequences reveals at least five clusters of conserved nucleotides; at least two clusters appear to be in excess of the minimal set usually associated with intron excision, but their functions are unknown. Two equally most-parsimonious (MP) trees were found when indels were not included in the phylogenetic analysis, and six such trees were found when indels were included. The Neighbor-Joining and maximum-likelihood trees were identical to each other and to one of the MP trees in each MP analysis. Indels, as well as nucleotide substitutions, are phylogenetically informative, and bootstrap support exceeded 90% for 21 of 24 inferred nodes when indels were included in the MP analysis. All traditional orders represented by two or more species appear monophyletic. Relationships among avian orders are strongly supported with the exception of an inferred sister-group relationship between Caprimulgiformes and Columbiformes. A relatively close relationship between Piciformes and Passeriformes is inferred, at odds with earlier DNA-DNA hybridization studies but consistent with traditional classifications. Among Passeriformes, the traditional perspective of a sister-group relationship of suboscines and oscines is supported, as is the subsequent split of the oscines into a lineage representative of the Corvida before the diversification of the Passerida. The four species of owls divide into two strongly supported clades, corresponding to the widely accepted bifurcation of owls into two families, Tytonidae and Strigidae. A sister-group relationship between gallinaceous birds and waterfowl, the Galloanserae, is also strongly supported.

[1]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[2]  E. Braun,et al.  Examining Basal avian divergences with mitochondrial sequences: model complexity, taxon sampling, and sequence length. , 2002, Systematic biology.

[3]  Alain Giron,et al.  A genomic schism in birds revealed by phylogenetic analysis of DNA strings. , 2002, Systematic biology.

[4]  T. Paton,et al.  Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  P. Ericson,et al.  A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  F. K. Barker,et al.  A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  W. Moore,et al.  A test of a mitochondrial gene-based phylogeny of woodpeckers (genus Picoides) using an independent nuclear gene, beta-fibrinogen intron 7. , 2002, Molecular phylogenetics and evolution.

[8]  J. Mattick,et al.  The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms. , 2001, Molecular biology and evolution.

[9]  D. G. Smith,et al.  Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. , 2001, Journal of human evolution.

[10]  A. Malhotra,et al.  Nuclear and mtDNA phylogenies of the Trimeresurus complex: implications for the gene versus species tree debate. , 2001, Molecular phylogenetics and evolution.

[11]  T. Parsons,et al.  Phylogeny of major lineages of suboscines (Passeriformes) analysed by nuclear DNA sequence data , 2001 .

[12]  S. Hedges,et al.  Calibration of avian molecular clocks. , 2001, Molecular biology and evolution.

[13]  K. Johnson,et al.  Taxon sampling and the phylogenetic position of Passeriformes: evidence from 916 avian cytochrome b sequences. , 2001, Systematic biology.

[14]  D. Mindell,et al.  Rooting a phylogeny with homologous genes on opposite sex chromosomes (gametologs): a case study using avian CHD. , 2000, Molecular biology and evolution.

[15]  I. Lovette,et al.  c-mos variation in songbirds: molecular evolution, phylogenetic implications, and comparisons with mitochondrial differentiation. , 2000, Molecular biology and evolution.

[16]  T. Parsons,et al.  Major Divisions in Oscines Revealed by Insertions in the Nuclear Gene c-myc: A Novel Gene in Avian Phylogenetics , 2000 .

[17]  M. A. Nedbal,et al.  Evidence from intron 1 of the nuclear transthyretin (Prealbumin) gene for the phylogeny of African mole-rats (Bathyergidae). , 2000, Molecular phylogenetics and evolution.

[18]  Kevin Burrage,et al.  ISIS, the intron information system, reveals the high frequency of alternative splicing in the human genome , 2000, Nature Genetics.

[19]  S. Hedges,et al.  The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes. , 2000, Molecular biology and evolution.

[20]  F. Ayala,et al.  Disparate Evolution of Paralogous Introns in the Xdh Gene of Drosophila , 2000, Journal of Molecular Evolution.

[21]  G. Barrowclough,et al.  Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. , 1999, Molecular phylogenetics and evolution.

[22]  M. Hasegawa,et al.  Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. , 1999, Systematic biology.

[23]  P J Waddell,et al.  Assessing the Cretaceous superordinal divergence times within birds and placental mammals by using whole mitochondrial protein sequences and an extended statistical framework. , 1999, Systematic biology.

[24]  W. Moore,et al.  Two-step cycle sequencing reduces premature terminations when using primers with high annealing temperatures , 1998, Molecular biotechnology.

[25]  W. Knöchel,et al.  Structural and functional analysis of the BMP-4 promoter in early embryos of Xenopus laevis , 1998, Mechanisms of Development.

[26]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[27]  W. Moore,et al.  The utility of DNA sequences of an intron from the beta-fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae). , 1997, Molecular phylogenetics and evolution.

[28]  A. Härlid,et al.  The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. , 1997, Molecular biology and evolution.

[29]  W. D. de Jong,et al.  alpha-Crystallin sequences support a galliform/anseriform clade. , 1997, Molecular phylogenetics and evolution.

[30]  D Penny,et al.  Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence , 1997, Science.

[31]  D. Swofford,et al.  Evolution of the Mitochondrial Cytochrome Oxidase II Gene in Collembola , 1997, Journal of Molecular Evolution.

[32]  F. Sheldon,et al.  A Reconsideration of Songbird Phylogeny, with Emphasis on the Evolution of Titmice and their Sylvioid Relatives , 1996 .

[33]  M. Goodman,et al.  Molecular phylogeny of the New World monkeys (Platyrrhini, primates) based on two unlinked nuclear genes: IRBP intron 1 and epsilon-globin sequences. , 1996, American journal of physical anthropology.

[34]  D. A. Kirby,et al.  Maintenance of pre-mRNA secondary structure by epistatic selection. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Feduccia Explosive Evolution in Tertiary Birds and Mammals , 1995, Science.

[36]  F. Lapointe,et al.  DNA-DNA hybridization-based phylogeny for "higher" nonpasserines: reevaluating a key portion of the avian family tree. , 1994, Molecular phylogenetics and evolution.

[37]  Ziheng Yang Estimating the pattern of nucleotide substitution , 1994, Journal of Molecular Evolution.

[38]  M. Steel,et al.  Recovering evolutionary trees under a more realistic model of sequence evolution. , 1994, Molecular biology and evolution.

[39]  C. Moritz,et al.  Multiple nuclear-gene phylogenies: application to pinnipeds and comparison with a mitochondrial DNA gene phylogeny. , 1994, Molecular biology and evolution.

[40]  J. Harshman Reweaving the Tapestry: What can We Learn from Sibley and Ahlquist (1990)? , 1994 .

[41]  S. Hedges,et al.  Molecular evidence for the origin of birds. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[42]  P. D. Jackson,et al.  Embryonic expression patterns of the drosophila decapentaplegic gene: Separate regulatory elements control blastoderm expression and lateral ectodermal expression , 1994, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  A. Clark,et al.  Conservation of alternative splicing and genomic organization of the myosin alkali light-chain (Mlc1) gene among Drosophila species. , 1993, Molecular biology and evolution.

[44]  Stephen M. Mount,et al.  Splicing signals in Drosophila: intron size, information content, and consensus sequences. , 1992, Nucleic acids research.

[45]  T. Tansey,et al.  A muscle-specific intron enhancer required for rescue of indirect flight muscle and jump muscle function regulates Drosophila tropomyosin I gene expression , 1991, Molecular and cellular biology.

[46]  A. Wilson,et al.  Mitochondrial resolution of a deep branch in the genealogical tree for perching birds , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  Jon E. Ahlquist,et al.  Phylogeny and Classification of the Birds: A Study in Molecular Evolution , 1991 .

[48]  D. Martindale,et al.  Nuclear pre-mRNA introns: analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. , 1990, Nucleic acids research.

[49]  M. Benton Phylogeny of the major tetrapod groups: Morphological data and divergence dates , 1990, Journal of Molecular Evolution.

[50]  M. Goodman,et al.  A molecular view of primate phylogeny and important systematic and evolutionary questions. , 1989, Molecular biology and evolution.

[51]  R. Renkawitz-Pohl,et al.  Intron and upstream sequences regulate expression of the Drosophila beta 3-tubulin gene in the visceral and somatic musculature, respectively. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Lanyon The Stochastic Mode of Molecular Evolution: What Consequences for Systematic Investigations? , 1988 .

[53]  William A. Noon,et al.  Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs , 1985, Nucleic Acids Res..

[54]  Michael R. Green,et al.  Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro , 1984, Cell.

[55]  J. Cracraft,et al.  THE RECENT BIRDS OF THE WORLD (CLASS AVES) , 1981 .

[56]  W. Bock THE PNEUMATIC FOSSA OF THE HUMERUS IN THE PASSERES , 1962 .

[57]  C. I. Bliss,et al.  FITTING THE NEGATIVE BINOMIAL DISTRIBUTION TO BIOLOGICAL DATA AND NOTE ON THE EFFICIENT FITTING OF THE NEGATIVE BINOMIAL , 1953 .

[58]  K. Miller,et al.  Sequence analysis of a polymorphic Mhc class II gene in Pacific salmon , 2005, Immunogenetics.

[59]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[60]  J. Dumbacher,et al.  Adenylate Kinase Intron 5: A New Nuclear Locus for Avian Systematics , 2001 .

[61]  D. Clayton,et al.  Nuclear and mitochondrial genes contain similar phylogenetic signal for pigeons and doves (Aves: Columbiformes). , 2000, Molecular phylogenetics and evolution.

[62]  D. Mindell,et al.  CHAPTER 8 – Phylogenetic Relationships among and within Select Avian Orders Based on Mitochondrial DNA , 1997 .

[63]  D. Mindell Avian molecular evolution and systematics , 1997 .

[64]  A. Clark,et al.  Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. , 1995, Genetics.

[65]  G. Bernardi,et al.  The human genome: organization and evolutionary history. , 1995, Annual review of genetics.

[66]  S. Lanyon,et al.  REEXAMINATION OF BARBET MONOPHYLY USING MITOCHONDRIAL-DNA SEQUENCE DATA , 1994 .

[67]  D. Mindell DNA-DNA hybridization and avian phylogeny , 1992 .

[68]  B. Monroe,et al.  Distribution and taxonomy of birds of the world , 1990 .

[69]  L. L. Short,et al.  Woodpeckers of the world , 1982 .

[70]  J. Cracraft,et al.  The Morphology of the Syrinx in Passerine Birds , 1972 .

[71]  A. Wetmore A classification for the birds of the world , 1960 .