Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression

Molecular Biology and Evolution

Volumn 32, Issue 4, 2015, Pages 871-887

  Opazo, Juan C ^a   Hoffmann, Federico G ^b,c   Natarajan, Chandrasekhar ^d   Witt, Christopher C ^e   Berenbrink, Michael ^f   Storz, Jay F ^d  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

^d UNIVERSITY OF NEBRASKA   (United States)

^e UNIVERSITY OF NEW MEXICO   (United States)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

avian genomics; gene deletion; gene duplication; gene family evolution; hemoglobin; protein evolution

Indexed keywords

HEMOGLOBIN; HEMOGLOBIN A; HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; HEMOGLOBIN D; AVIAN PROTEIN; ISOPROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BAYES THEOREM; BIRD; CHARADRIIFORMES; CHICKEN; CLADISTICS; EMBRYO DEVELOPMENT; ERYTHROCYTE; FAMILY; GENE CLUSTER; GENE CONVERSION; GENE DOSAGE; GENE STRUCTURE; GENETIC VARIABILITY; GLOBIN GENE; HEMOGLOBIN SYNTHESIS; IN VITRO STUDY; MONOPHYLY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PENGUIN; PHYLOGENY; PIGEONS AND DOVES; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PSEUDOGENE; PSITTACINE; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; TAENIOPYGIA GUTTATA; VULTURE (BIRD); ANIMAL; GENETICS; GENOMICS; MOLECULAR EVOLUTION;

AVES; MAMMALIA;

ALPHA-GLOBINS; ANIMALS; AVIAN PROTEINS; BETA-GLOBINS; BIRDS; EVOLUTION, MOLECULAR; GENE DOSAGE; GENOMICS; MULTIGENE FAMILY; PHYLOGENY; PROTEIN ISOFORMS;

EID: 84988304467     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu341     Document Type: Article

References (114)

1. Abramoff MD, Magelhaes PJ, Ram SJ.(2004).Image processing with image.J Biophoton Int.11:36-42
2. Alev C, McIntyre BAS, Nagai H, Shin M, Shinmyozu K, Jakt LM, Sheng G.(2008).bA, the major b-globin in definitive red blood cells, is present from the onset of primitive erythropoiesis in chicken.Dev Dyn.237: 1193-1197
3. Alev C, Shinmyozu K, McIntyre BAS, Sheng G.(2009).Genomic organization of zebra finch a and b globin genes and their expression in primitive and definitive blood in comparison with globins in chicken.Dev Genes .Evol.219:353-360
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ.(1990).Basic local alignment search tool.J Mol Biol.215:403-410
5. Backstrom N, Karaiskou N, Leder EH, Gustafsson L, Primmer CR, Qvarnstrom A, Ellegren H.(2008).A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution.Genetics 179:1479-1495
6. Baumann FH, Baumann HR.(1977).A comparative study of oxygen transport in bird blood.Respir Physiol.31:333-343
7. Berenbrink M.(2006).Evolution of vertebrate haemoglobins: histidine side chains, specific buffer value and Bohr effect.Respir Physiol Neurobiol.154:165-184
8. Berenbrink M.(2007).Historical reconstructions of evolving physiological complexity: O2 secretion in the eye and swimbladder of fishes.J Exp Biol.210:1641-1652
9. Berenbrink M, Koldkjaer P, Kepp O, Cossins AR.(2005).Evolution of oxygen secretion in fishes and the emergence of a complex physiological system.Science 307:1752-1757
10. Blank M, Kiger L, Thielebein A, Gerlach F, Hankeln T, Marden MC, Burmester T.(2011).Oxygen supply from the bird's eye perspective: globin E is a respiratory protein in the chicken retina.J Biol Chem.286:26507-26515
11. Blomberg SP, Garland T, Ives AR.(2003).Testing for phylogenetic signal in comparative data: behavioral traits are more labile.Evolution 57: 717-745
12. Bunn HF.(1980).Regulation of hemoglobin-function in mammals.Am Zool.20:199-211
13. Bunn HF.(1987).Subunit assembly of hemoglobin: an important determinant of hematologic phenotype.Blood 69:1-6
14. Bunn HF, McDonald MJ.(1983).Electrostatic interactions in the assembly of haemoglobin.Nature 306:498-500
15. Burge C, Karlin S.(1997).Prediction of complete gene structures in human genomic DNA.J Mol Biol.268:78-94
16. Burmester T, Hankeln T.(2014).Function and evolution of vertebrate globins.Acta Physiol.211:501-514
17. Burt DW, Bruley C, Dunn IC, Jones CT, Ramage A, Law AS, Morrice DR, Paton IR, Smith J, Windsor D, et al.(1999).The dynamics of chromosome evolution in birds and mammals.Nature 402:411-413
18. Cheviron ZA, Natarajan C, Projecto-Garcia J, Eddy DK, Jones J, Carling MD, Witt CC, Moriyama H, Weber RE, Fago A, et al.(2014).Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean sparrow, Zonotrichia capensis.Mol Biol Evol.31: 2948-2962
19. Cirotto C, Panara F, Arangi I.(1987).The minor hemoglobins of primitive and definitive erythrocytes of the chicken embryo-evidence for Hemoglobin-L.Development 101:805-813
20. Cobb JA, Manning D, Kolatkar PR, Cox DJ, Riggs AF.(1992).Deoxygenation-linked association of a tetrameric component of chicken hemoglobin.J Biol Chem.267:1183-1189
21. Cooper SJB, Wheeler D, De Leo A, Cheng JF, Holland RAB, Graves JAM, Hope RM.(2006).The mammalian aD-globin gene lineage and a new model for the molecular evolution of a-globin gene clusters at the stem of the mammalian radiation.Mol Phylogenet Evol.38:439-448
22. Dalloul RA, Long JA, Zimin AV, Aslam L, Beal K, Blomberg LA, Bouffard P, Burt DW, Crasta O, Crooijmans RPMA, et al.(2010).Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis.PLoS Biol.8(9):e1000475
23. Damsgaard C, Storz JF, Hoffmann FG, Fago A.(2013).Hemoglobin isoform differentiation and allosteric regulation of oxygen binding in the turtle, Trachemys scripta.Am J Physiol Regul Integr Comp Physiol.305:R961-R967
24. Derjusheva S, Kurganova A, Habermann F, Gaginskaya E.(2004).High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds.Chromosome Res.12:715-723
25. Dunning JBJ.(2008).CRC Handbook of avian body masses.Boca Raton (FL): CRC Press
26. Ellegren H.(2013).The evolutionary genomics of birds.Ann Rev Ecol Evol Syst.44:239-259
27. Ellegren H.(2010).Evolutionary stasis: the stable chromosomes of birds.Trends Ecol Evol.25:283-291
28. Fair JM, Paul E.(2010).Guidelines to the use of wild birds in research.Washington (DC): Ornithological Council
29. Fronticelli C, Teresa Sana M, Perez-Alvarado GC, Karavitis M, Lu A-L, Brinigar WS.(1995).Allosteric modulation by tertiary structure in mammalian Hbs.J.Biol Chem.270:30588-30592
30. Fuchs C, Burmester T, Hankeln T.(2006).The amphibian globin gene repertoire as revealed by the Xenopus genome.Cytogenet Genome Res.112:296-306
31. Garland T, Bennett AF, Rezende EL.(2005).Phylogenetic approaches in comparative physiology.J Exp Biol.208:3015-3035
32. Gaudry MJ, Storz JF, Butts GT, Campbell KL, Hoffman FG.(2014).Repeated evolution of chimeric fusion genes in the b-globin gene family of laurasiatherian mammals.Genome Biol Evol.6:1219-1233
33. Gillemans N, McMorrow T, Tewari R, Wai AWK, Burgtorf C, Drabek D, Ventress N, Langeveld A, Higgs D, Tan-Un K, et al.(2003).Functional and comparative analysis of globin loci in pufferfish and humans.Blood 101:2842-2849
34. Goh SH, Lee YT, Bhanu NV, Cam MC, Desper R, Martin BM, Moharram R, Gherman RB, Miller JL.(2005).A newly discovered human a-globin gene.Blood 106:1466-1472
35. Goldman N, Yang ZH.(1994).Codon-based model of nucleotide substitution for protein-coding DNA sequences.Mol Biol Evol.11:725-736
36. Goodman M.(1963).Man's place in the phylogeny of the primates as reflected in serum proteins.In: Washburn S, editor.Classification and human evolution.Chicago (IL): Viking Fund Publications.p.204-230
37. Griffin DK, Robertson LB, Tempest HG, Vignal A, Fillon V, Crooijmans RPMA, Groenen MAM, Deryusheva S, Gaginskaya E, Carre W, et al.(2008).Whole genome comparative studies between chicken and turkey and their implications for avian genome evolution.BMC Genomics 9:168
38. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St John JA, Capella-Gutiérrez S, Castoe TA, et al.(2014).Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs.Science 346:1335
39. Griffin DK, Robertson LBW, Tempest HG, Skinner BM.(2007).The evolution of the avian genome as revealed by comparative molecular cytogenetics.Cytogenet Genome Res.117:64-77
40. Grigg GC, Wells RMG, Beard LA.(1993).Allosteric control of oxygen binding by hemoglobin during embryonic development in the crocodile Crocodylus porosus-The role of red-cell organic phosphates and carbon dioxide.J Exp Biol.175:15-32
41. Grispo MT, Natarajan C, Projecto-Garcia J, Moriyama H, Weber RE, Storz JF.(2012).Gene duplication and the evolution of hemoglobin isoform differentiation in birds.J Biol Chem.287:37647-37658
42. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, et al.(2008).A phylogenomic study of birds reveals their evolutionary history.Science 320:1763-1768
43. Hahn MW, De Bie T, Stajich JE, Nguyen C, Cristianini N.(2005).Estimating the tempo and mode of gene family evolution from comparative genomic data.Genome Res.15:1153-1160
44. Han MV, Thomas GWC, Lugo-Martinez J, Hahn MW.(2013).Estimating gene gain and loss rates in the presence of genome assembly and annotation error using CAFE 3.Mol Biol Evol.30:1987-1997
45. Hardison RC.(2001).Organization, evolution and regulation of the globin genes.In: Steinberg MH, Forget BG, Higgs DR, Nagel RL, editors.Disorders of hemoglobin: genetics, pathophysiology and clinical management.Cambridge: Cambridge University Press.p.95-115
46. Hardison RC.(2008).Globin genes on the move.J Biol.7:35
47. Hardison RC.(2012).Evolution of hemoglobin and its genes.Cold Spring Harb Perspect Med.2:a011627
48. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W.(2008).GEIGER: investigating evolutionary radiations.Bioinformatics 24: 129-131
49. Hiebl I, Weber RE, Schneeganss D, Kosters J, Braunitzer G.(1988).Highaltitude respiration of birds-structural adaptations in the major andminor hemoglobin components of adult Ruppells griffon (Gryps rueppellii)-A new molecular pattern for hypoxia tolerance.Biol Chem Hoppe-Seyler.369:217-232
50. Hillier LW, Miller W, Birney E, Warren W, Hardison RC, Ponting CP, Bork P, Burt DW, Groenen MAM, Delany ME, et al.(2004).Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.Nature 432:695-716
51. Hoffmann FG, Opazo JC, Hoogewijs D, Hankeln T, Ebner B, Vinogradov SN, Bailly X, Storz JF.(2012).Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition.Mol Biol Evol.29:1735-1745
52. Hoffmann FG, Opazo JC, Storz JF.(2008).New genes originated via multiple recombinational pathways in the b-globin gene family of rodents.Mol Biol Evol.25:2589-2600
53. Hoffmann FG, Opazo JC, Storz JF.(2008).Rapid rates of lineage-specific gene duplication and deletion in the a-globin gene family.Mol Biol Evol.25:591-602
54. Hoffmann FG, Opazo JC, Storz JF.(2010).Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates.Proc Natl Acad Sci U S A.107:14274-14279
55. Hoffmann FG, Opazo JC, Storz JF.(2011).Differential loss and retention of cytoglobin, myoglobin, and globin-E during the radiation of vertebrates.Genome Biol Evol.3:588-600
56. Hoffmann FG, Opazo JC, Storz JF.(2012).Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates.Mol Biol Evol.29:303-312
57. Hoffmann FG, Storz JF.(2007).The aD-globin gene originated via duplication of an embryonic a-like globin gene in the ancestor of tetrapod vertebrates.Mol Biol Evol.24:1982-1990
58. Hoffmann FG, Storz JF, Gorr TA, Opazo JC.(2010).Lineage-specific patterns of functional diversification in the a-And b-globin gene families of tetrapod vertebrates.Mol Biol Evol.27:1126-1138
59. Hoogewijs D, Ebner B, Germani F, Hoffmann FG, Fabrizius A, Moens L, Burmester T, Dewilde S, Storz JF, Vinogradov SN, et al.(2012).Androglobin: a chimeric globin in metazoans that is preferentially expressed in mammalian testes.Mol Biol Evol.29:1105-1114
60. Hosbach HA, Wyler T, Weber R.(1983).The Xenopus laevis globin gene family-chromosomal arrangement and gene structure.Cell 32: 45-53
61. Huang Y, Li Y, Burt DW, Chen H, Zhang Y, Qian W, Kim H, Gan S, Zhao Y, Li J, et al.(2013).The duck genome and transcriptome provide insight into an avian influenza virus reservoir species.Nature Genet.45:776-783
62. Ikehara T, Eguchi Y, Kayo S, Takei H.(1997).Isolation and sequencing of two a-globin genes a(A) and a(D) in pigeon and evidence for embryo-specific expression of the a(D)-globin gene.Biochemical and Biophys Res Commun.234:450-453
63. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, et al.(2014).Whole genome analyses resolve early branches in the tree of life of modern birds.Science 346: 1320-1331
64. Jeffreys AJ, Wilson V, Wood D, Simons JP, Kay RM, Williams JG.(1980).Linkage of adult a-globin and b-globin genes in X laevis and gene duplication by tetraploidization.Cell 21:555-564
65. Jessen TH, Weber RE, Fermi G, Tame J, Braunitzer G.(1991).Adaptation of bird hemoglobins to high-Altitudes-demonstration of molecular mechanism by protein engineering.Proc Natl Acad Sci U S A.88: 6519-6522
66. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO.(2012).The global diversity of birds in space and time.Nature 491:444-448
67. Jobb G, von Haeseler A, Strimmer K.(2004).TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics.BMC Evol Biol.4:18
68. Katoh K, Toh H.(2008).Recent developments in the MAFFT multiple sequence alignment program.Brief Bioinform.9:286-298
69. Knapp JE, Oliveira MA, Xie Q, Ernst SR, Riggs AF, Hackert ML.(1999).The structural and functional analysis of the hemoglobin D component from chicken.J Biol Chem.274:6411-6420
70. Lutz PL.(1980).On the oxygen-Affinity of bird blood.Am Zool.20: 187-198
71. Lutz PL, Longmuir IS, Schmidt-Nielsen K.(1974).Oxygen affinity of bird blood.Respir Physiol.17:269-275
72. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TLL, Stadler T, et al.(2011).Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification.Science 334:521-524
73. Mindell DP, Knight A, Baer C, Huddleston CJ.(1996).Slow rates of molecular evolution in birds and the metabolic rate and body temperature hypotheses.Mol Biol Evol.13:422-426
74. Mrabet NT, McDonald MJ, Turci S, Sarkar R, Szabo A, Bunn HF.(1986).Electrostatic attraction governs the dimer assembly of human hemoglobin.J Biol Chem.261:5222-5228
75. Nam K, Mugal C, Nabholz B, Schielzeth H, Wolf JBW, Backstrom N, Kunstner A, Balakrishnan CN, Heger A, Ponting CP, et al.(2010).Molecular evolution of genes in avian genomes.Genome Biol.11:R68
76. Natarajan C, Inoguchi N, Weber RE, Fago A, Moriyama H, Storz JF.(2013).Epistasis among adaptive mutations in deer mouse hemoglobin.Science 340:1324-1327
77. Opazo JC, Butts GT, Nery MF, Storz JF, Hoffmann FG.(2013).Wholegenome duplication and the functional diversification of teleost fish hemoglobins.Mol Biol Evol.30:140-153
78. Opazo JC, Hoffmann FG, Storz JF.(2008).Differential loss of embryonic globin genes during the radiation of placental mammals.Proc Natl Acad Sci U S A.105:12950-12955
79. Opazo JC, Hoffmann FG, Storz JF.(2008).Genomic evidence for independent origins of b-like globin genes in monotremes and therian mammals.Proc Natl Acad Sci U S A.105:1590-1595
80. Opazo JC, Sloan AM, Campbell KL, Storz JF.(2009).Origin and ascendancy of a chimeric fusion gene: the b/-globin gene of paenungulate mammals.Mol Biol Evol.26:1469-1478
81. Pagel M.(1999).Inferring the historical patterns of biological evolution.Nature 401:877-884
82. Paradis E, Claude J, Strimmer K.(2004).APE: analyses of phylogenetics and evolution in R language.Bioinformatics 20:289-290
83. Patel VS, Cooper SJB, Deakin JE, Fulton B, Graves T, Warren WC, Wilson RK, Graves JAM.(2008).Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals.BMC Biol.6:34
84. Projecto-Garcia J, Natarajan C, Moriyama H, Weber RE, Fago A, Cheviron ZA, Dudley R, McGuire JA, Witt CC, Storz JF.(2013).Repeated elevational transitions in hemoglobin function during the evolution of Andean hummingbirds.Proc Natl Acad Sci U S A.110:20669-20674
85. Rana MS, Riggs AF.(2011).Indefinite noncooperative self-Association of chicken deoxy hemoglobin D.Proteins Struct Funct Bioinform.79: 1499-1512
86. Reitman M, Grasso JA, Blumenthal R, Lewit P.(1993).Primary sequence, evolution, and repetitive elements of the Gallus gallus (chicken) b-globin cluster.Genomics 18:616-626
87. Riggs AF.(1998).Self-Association, cooperativity and supercooperativity of oxygen binding by hemoglobins.J Exp Biol.201:1073-1084
88. Ronquist F, Huelsenbeck JP.(2003).MrBayes 3: Bayesian phylogenetic inference under mixed models.Bioinformatics 19:1572-1574
89. Runck AM, Moriyama H, Storz JF.(2009).Evolution of duplicated b-globin genes and the structural basis of hemoglobin isoform differentiation in Mus.Mol Biol Evol.26:2521-2532
90. Schmidt-Nielsen K, Larimer JL.(1958).Oxygen dissociation curves ofmammalian blood in relation to body size.Am J Physiol.195:424-428
91. Schwarze K, Burmester T.(2013).Conservation of globin genes in the "living fossil" Latimeria chalumnae and reconstruction of the evolution of the vertebrate globin family.Biochim Biophys Acta-Proteins Proteomics.1834:1801-1812
92. Schwarze K, Campbell KL, Hankeln T, Storz JF, Hoffman FG, Burmester T.(2014).The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates.Mol Biol Evol.31:2708-2721
93. Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N, Abramyan J, Amemiya CT, Badenhorst D, Biggar KK, et al.(2013).The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage.Genome Biol.14:R28
94. Shetty S, Griffin DK, Graves JAM.(1999).Comparative painting reveals strong chromosome homology over 80 million years of bird evolution.Chromosome Res.7:289-295
95. Shimodaira H.(2002).An approximately unbiased test of phylogenetic tree selection.Syst Biol.51:492-508
96. Sibly RM, Witt CC, Wright NA, Venditti C, Jetz W, Brown JH.(2012).Energetics, lifestyle, and reproduction in birds.Proc Natl Acad Sci U S A.109:10937-10941
97. Song G, Hsu C-H, Riemer C, Zhang Y, Kim HL, Hoffmann F, Zhang L, Hardison RC, Green ED, Miller W, et al.(2011).Conversion events in gene clusters.BMC Evol Biol.11:226
98. Song G, Riemer C, Dickins B, Kim HL, Zhang L, Zhang Y, Hsu C-H, Hardison RC, Nisc Comparative Sequencing P, Green ED, et al.(2012).Revealing mammalian evolutionary relationships by comparative analysis of gene clusters.Genome Biol Evol.4:586-601
99. Storz JF, Hoffmann FG, Opazo JC, Moriyama H.(2008).Adaptive functional divergence among triplicated a-globin genes in rodents.Genetics 178:1623-1638
100. Storz JF, Hoffmann FG, Opazo JC, Sanger TJ, Moriyama H.(2011).Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis.J Exp Biol.214:575-581
101. Storz JF, Opazo JC, Hoffmann FG.(2011).Phylogenetic diversification of the globin gene superfamily in chordates.IUBMB Life.63: 313-322
102. Storz JF, Opazo JC, Hoffmann FG.(2013).Gene duplication, genome duplication, and the functional diversification of vertebrate globins.Mol Phylogenet Evol.66:469-478
103. Tatusova TA, Madden TL.(1999).BLAST 2 SEQUENCES, a new tool for comparing protein and nucleotide sequences.FEMS Microbiol Lett.174:247-250
104. Tufts DM, Natarajan C, Revsbech IG, Projecto-Garcia J, Hoffmann FG, Weber RE, Fago A, Moriyama H, Storz JF.(2015).Epistasis constrains mutational pathways of hemoglobin adaptation in high-Altitude pikas.Mol Biol Evol.32(2):287-298
105. Weber RE, Fago A, Malte H, Storz JF, Gorr TA.(2013).Lack of conventional oxygen-linked proton and anion binding sites does not impair allosteric regulation of oxygen binding in dwarf caiman hemoglobin.Am J Physiol Regul Integr Comp Physiol.305:R300-R312
106. Weber RE, Jessen TH, Malte H, Tame J.(1993).Mutant hemoglobins (a(119)-Ala and b(55)-Ser)-functions related to high-Altitude respiration in geese.J Appl Physiol.75:2646-2655
107. Weber RE, Voelter W, Fago A, Echner H, Campanella E, Low PS.(2004).Modulation of red cell glycolysis: interactions between vertebrate hemoglobins and cytoplasmic domains of band 3 red cell membrane proteins.Am J Physiol Regul Integr Comp Physiol.287: R454-R464
108. Weber RE, White FN.(1986).Oxygen binding in alligator blood related to temperature, diving, and alkaline tide.Am J Physiol.251:R901-R908
109. Weber RE, White FN.(1994).Chloride-dependent organic phosphate sensitivity of the oxygenation reaction in crocodilian hemoglobins.J Exp Biol.192:1-11
110. Yang Z.(2007).PAML 4: phylogenetic analysis by maximum likelihood.Mol Biol Evol.24:1586-1591
111. Yang ZH.(1998).Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.Mol Biol Evol.15: 568-573
112. Yang ZH, Wong WSW, Nielsen R.(2005).Bayes empirical Bayes inference of amino acid sites under positive selection.Mol Biol Evol.22: 1107-1118
113. Zhan X, Pan S, Wang J, Dixon A, He J, Muller MG, Ni P, Hu L, Liu Y, Hou H, et al.(2013).Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle.Nat Genet.45: 563-566
114. Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, et al.(2014).Comparative genomics reveals insights into avian genome evolution and adaptation.Science 346:1311-1320