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Biology  2013 

Parsimony and Model-Based Analyses of Indels in Avian Nuclear Genes Reveal Congruent and Incongruent Phylogenetic Signals

DOI: 10.3390/biology2010419

Keywords: bird classification, avian phylogeny, nucleotide sequence alignment, total evidence, Columbiformes, Coraciiformes, Galliformes

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Abstract:

Insertion/deletion (indel) mutations, which are represented by gaps in multiple sequence alignments, have been used to examine phylogenetic hypotheses for some time. However, most analyses combine gap data with the nucleotide sequences in which they are embedded, probably because most phylogenetic datasets include few gap characters. Here, we report analyses of 12,030 gap characters from an alignment of avian nuclear genes using maximum parsimony (MP) and a simple maximum likelihood (ML) framework. Both trees were similar, and they exhibited almost all of the strongly supported relationships in the nucleotide tree, although neither gap tree supported many relationships that have proven difficult to recover in previous studies. Moreover, independent lines of evidence typically corroborated the nucleotide topology instead of the gap topology when they disagreed, although the number of conflicting nodes with high bootstrap support was limited. Filtering to remove short indels did not substantially reduce homoplasy or reduce conflict. Combined analyses of nucleotides and gaps resulted in the nucleotide topology, but with increased support, suggesting that gap data may prove most useful when analyzed in combination with nucleotide substitutions.

References

[1]  DeBry, R.W.; Seshadri, S. Nuclear intron sequences for phylogenetics of closely related mammals: An example using the phylogeny of Mus. J. Mammal. 2001, 82, 280–288, doi:10.1644/1545-1542(2001)082<0280:NISFPO>2.0.CO;2.
[2]  Kimball, R.T.; Braun, E.L.; Ligon, J.D.; Randi, E.; Lucchini, V. A molecular phylogeny of the Peacock-pheasants (Galliformes: Polyplectron spp.) indicates loss and reduction of ornamental traits and display behaviors. Biol. J. Linn. Soc. 2001, 73, 187–198.
[3]  Creer, S.; Malhotra, A.; Thorpe, R.S.; Pook, C.E. Targeting optimal introns for phylogenetic analyses in non-model taxa: Experimental results in Asian pitvipers. Cladistics 2005, 21, 390–395.
[4]  Benavides, E.; Baum, R.; McClellan, D.; Sites, J.W. Molecular phylogenetics of the lizard genus Microlophus (Squamata: Tropiduridae): Aligning and retrieving indel signal from nuclear introns. Syst. Biol. 2007, 56, 776–797, doi:10.1080/10635150701618527.
[5]  Igea, J.; Juste, J.; Castresana, J. Novel intron markers to study the phylogeny of closely related mammalian species. BMC Evol. Biol. 2010, 10, 369.
[6]  Harshman, J.; Huddleston, C.J.; Bollback, J.P.; Parsons, T.J.; Braun, M.J. True and false gharials: A nuclear gene phylogeny of Crocodylia. Syst. Biol. 2003, 52, 386–402.
[7]  Kimball, R.T.; Braun, E.L. A multigene phylogeny of Galliformes supports a single origin of erectile ability in non-feathered facial traits. J. Avian Biol. 2008, 39, 438–445.
[8]  Bonilla, A.J.; Braun, E.L.; Kimball, R.T. Comparative molecular evolution and phylogenetic utility of 3'-UTRs and introns in Galliformes. Mol. Phylogenet. Evol. 2010, 56, 536–542, doi:10.1016/j.ympev.2010.04.006.
[9]  Prychitko, T.M.; Moore, W.S. Alignment and phylogenetic analysis of β-Fibrinogen intron 7 sequences among avian orders reveal conserved regions within the intron. Mol. Biol. Evol. 2003, 20, 762–771, doi:10.1093/molbev/msg080.
[10]  Fain, M.G.; Houde, P. Parallel radiations in the primary clades of birds. Evolution 2004, 58, 2558–2573.
[11]  Matthee, C.A.; Eick, G.; Willows-Munro, S.; Montgelard, C.; Pardini, A.T.; Robinson, T.J. Indel evolution of mammalian introns and the utility of non-coding nuclear markers in eutherian phylogenetics. Mol. Phylogenet. Evol. 2007, 42, 827–837, doi:10.1016/j.ympev.2006.10.002.
[12]  Chojnowski, J.L.; Kimball, R.T.; Braun, E.L. Introns outperform exons in analyses of basal avian phylogeny using clathrin heavy chain genes. Gene 2008, 410, 89–96.
[13]  Hackett, S.J.; Kimball, R.T.; Reddy, S.; Bowie, R.C.K.; Braun, E.L.; Braun, M.J.; Chojnowski, J.L.; Cox, W.A.; Han, K.-L.; Harshman, J.; et al. A phylogenomic study of birds reveals their evolutionary history. Science 2008, 320, 1763–1768.
[14]  Giribet, G.; Wheeler, W.C. On gaps. Mol. Phylogenet. Evol. 1999, 13, 132–143, doi:10.1006/mpev.1999.0643.
[15]  Kjer, K.M.; Gillespie, J.J.; Ober, K.A. Opinions on multiple sequence alignment, and an empirical comparison of repeatability and accuracy between POY and structural alignment. Syst. Biol. 2007, 56, 133–146, doi:10.1080/10635150601156305.
[16]  Morrison, D.A. Why would phylogeneticists ignore computerized sequence alignment? Syst. Biol. 2009, 58, 150–158, doi:10.1093/sysbio/syp009.
[17]  Lee, J.Y.; Joseph, L.; Edwards, S.V. A species tree for the Australo-Papuan Fairy-wrens and allies (Aves: Maluridae). Syst. Biol. 2012, 61, 253–271.
[18]  Saurabh, K.; Holland, B.R.; Gibb, G.C.; Penny, D. Gaps: An elusive source of phylogenetic information. Syst. Biol. 2012, 61, 1075–1082, doi:10.1093/sysbio/sys043.
[19]  Simmons, M.P.; Ochoterena, H. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 2000, 49, 369–381.
[20]  Simmons, M.P.; Ochoterena, H.; Carr, T.G. Incorporation, relative homoplasy, and effect of gap characters in sequence-based phylogenetic analyses. Syst. Biol. 2001, 50, 454–462.
[21]  Dwivedi, B.; Gadagkar, S.R. Phylogenetic inference under varying proportions of indel-induced alignment gaps. BMC Evol. Biol. 2009, 9, 211, doi:10.1186/1471-2148-9-211.
[22]  Warnow, T. Standard maximum likelihood analyses of alignments with gaps can be statistically inconsistent. PLoS Curr. 2012, 4, RN1308, doi:10.1371/currents.RRN1308.
[23]  Lake, J.A. The order of sequence alignment can bias the selection of tree topology. Mol. Biol. Evol. 1991, 8, 378–385.
[24]  Ogden, T.H.; Rosenberg, M.S. Multiple sequence alignment accuracy and phylogenetic inference. Syst. Biol. 2006, 55, 314–328.
[25]  Smythe, A.B.; Sanderson, M.J.; Nadler, S.A. Nematode small subunit phylogeny correlates with alignment parameters. Syst. Biol. 2006, 55, 972–992, doi:10.1080/10635150601089001.
[26]  Liu, K.; Raghavan, S.; Nelesen, S.; Linder, C.R.; Warnow, T. Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 2009, 324, 1561–1564, doi:10.1126/science.1171243.
[27]  Liu, K.; Linder, C.R.; Warnow, T. Multiple sequence alignment: A major challenge to large-scale phylogenetics. PLoS Curr. 2010, 2, RN1198.
[28]  Pratt, R.C.; Gibb, G.C.; Morgan-Richards, M.; Phillips, M.J.; Hendy, M.D.; Penny, D. Toward resolving deep Neoaves phylogeny: Data, signal enhancement, and priors. Mol. Biol. Evol. 2009, 26, 313–326.
[29]  Phillips, M.J.; Gibb, G.C.; Crimp, E.A.; Penny, D. Tinamous and Moa flock together: Mitochondrial genome sequence analysis reveals independent losses of flight among ratites. Syst. Biol. 2010, 59, 90–107, doi:10.1093/sysbio/syp079.
[30]  Wang, N.; Braun, E.L.; Kimball, R.T. Testing hypotheses about the sister group of the Passeriformes using an independent 30 locus dataset. Mol. Biol. Evol. 2012, 29, 737–750.
[31]  Smith, J.V.; Braun, E.L.; Kimball, R.T. Ratite non-monophyly: Independent evidence from 40 novel loci. Syst. Biol. 2013, 62, 35–49, doi:10.1093/sysbio/sys067.
[32]  Golenberg, E.M.; Clegg, M.T.; Durbin, M.L.; Doebley, J.; Ma, D.P. Evolution of a noncoding region of the chloroplast genome. Mol. Phylogenet. Evol. 1993, 2, 52–64, doi:10.1006/mpev.1993.1006.
[33]  Regier, J.C.; Zwick, A. Sources of signal in 62 protein-coding nuclear genes for higher-level phylogenetics of arthropods. PLoS One 2011, 6, e23408.
[34]  Belinky, F.; Cohen, O.; Huchon, D. Large-scale parsimony analysis of metazoan indels in protein-coding genes. Mol. Biol. Evol. 2010, 27, 441–451.
[35]  Braun, E.L.; Kimball, R.T.; Han, K.-L.; Iuhasz-Velez, N.R.; Bonilla, A.J.; Chojnowski, J.L.; Smith, J.V.; Bowie, R.C.K.; Braun, M.J.; Hackett, S.J.; et al. Homoplastic microinversions and the avian tree of life. BMC Evol. Biol. 2011, 11, 141.
[36]  Yang, Z. On the best evolutionary rate for phylogenetic analysis. Syst. Biol. 1998, 47, 125–133, doi:10.1080/106351598261067.
[37]  Braun, E.L.; Kimball, R.T. Polytomies, the power of phylogenetic inference, and the stochastic nature of molecular evolution: A comment on Walsh et al. (1999). Evolution 2001, 55, 1261–1263.
[38]  Ericson, P.G.P.; Elzanowski, A. Phylogenetic utility and evolution of indels: A study in neognathous birds. Mol. Phylogenet. Evol. 2011, 61, 760–771, doi:10.1016/j.ympev.2011.07.021.
[39]  Wolf, Y.I.; Rogozin, I.B.; Koonin, E.V. Coelomata and not Ecdysozoa: Evidence from genome-wide phylogenetic analysis. Genome Res. 2004, 14, 29–36.
[40]  Kimball, R.T.; Braun, E.L.; Bowie, R.C.K.; Braun, M.J.; Chojnowski, J.L.; Hackett, S.J.; Han, K.-L.; Harshman, J.; Heimer-Torres, V.; Holznagel, W.; et al. A set of resources to amplify nuclear regions across the avian genome. Mol. Phylogenet. Evol. 2009, 50, 654–660, doi:10.1016/j.ympev.2008.11.018.
[41]  Shetty, S.; Griffin, D.K.; Graves, J.A.M. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res. 1999, 7, 289–295, doi:10.1023/A:1009278914829.
[42]  Yuri, T.; Kimball, R.T.; Braun, E.L.; Braun, M.J. Duplication and accelerated evolution of growth hormone gene in passerine birds. Mol. Biol. Evol. 2008, 25, 352–361.
[43]  Müller, K. SeqState: Primer design and sequence statistics for phylogenetic DNA datasets. Appl. Bioinformatics 2005, 4, 65–69, doi:10.2165/00822942-200504010-00008.
[44]  Reddy, S.; Braun, E.L. Assembling the Tree of Life: Early Bird. Available online: http://www.biology.ufl.edu/earlybird/ (accessed on 21 February 2013).
[45]  Swofford, D.L. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b10; Sinauer Associates: Sunderland, MA, USA, 2007.
[46]  Nixon, K.C. The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics 1999, 15, 407–414, doi:10.1111/j.1096-0031.1999.tb00277.x.
[47]  Cavender, J.A. Taxonomy with confidence. Math. Biosci. 1978, 40, 271–280.
[48]  Farris, J.S. Probability model for inferring evolutionary trees. Syst. Zool. 1973, 22, 250–256.
[49]  Neyman, J. Molecular studies of evolution: A source of novel statistical problems. In Molecular Studies of Evolution: A Source of Novel Statistical Problems; Gupta, S.S., Yackel, J., Eds.; New York Academic Press: New York, NY, USA, 1971; pp. 1–27.
[50]  Lewis, P.O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 2001, 50, 913–925.
[51]  Felsenstein, J. Phylogenies from restriction sites: A maximum-likelihood approach. Evolution 1992, 46, 156–173.
[52]  Zwickl, D.J. Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological under the Maximum Likelihood Criterion; The University of Texas at Austin: Austin, TX, USA, 2006.
[53]  Russo, C.A.M.; Takezaki, N.; Nei, M. Efficiencies of different genes and different tree-building methods in recovering a known vertebrate phylogeny. Mol. Biol. Evol. 1996, 13, 525–536.
[54]  Miyamoto, M.M.; Fitch, W.M. Testing species phylogenies and phylogenetic methods with congruence. Syst. Biol. 1995, 44, 64–76.
[55]  H?stad, O.; Bj?rklund, M. Nucleotide substitution models and estimation of phylogeny. Mol. Biol. Evol. 1998, 15, 1381–1389, doi:10.1093/oxfordjournals.molbev.a025866.
[56]  Harshman, J. Classification and phylogeny of birds. In Reproductive Biology and Phylogeny of Birds; Jamieson, B.G.M., Ed.; Science Publishers: Enfield, NH, USA, 2007; pp. 1–35.
[57]  Clements, J.F.; Schulenberg, T.S.; Iliff, M.J.; Sullivan, B.L.; Wood, C.L.; Roberson, D. The Clements Checklist of Birds of the World: Version 6.6. Available online: http://www.birds.cornell.edu/clementschecklist/downloadable-clements-checklist/ (accessed on 12 August 2012).
[58]  Gill, F.; Donsker, D. IOC World Bird Names (v 3.2). Available online: http://www.worldbirdnames.org/ (accessed on 12 November 2012).
[59]  Pacheco, M.A.; Battistuzzi, F.U.; Lentino, M.; Aguilar, R.F.; Kumar, S.; Escalante, A.A. Evolution of modern birds revealed by mitogenomics: Timing the radiation and origin of major orders. Mol. Biol. Evol. 2011, 28, 1927–1942, doi:10.1093/molbev/msr014.
[60]  Suh, A.; Paus, M.; Kiefmann, M.; Churakov, G.; Franziska, A.F.; Brosius, J.; Kriegs, J.O.; Schmitz, J. Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat. Commun. 2011, 2, 443, doi:10.1038/ncomms1448.
[61]  Matzke, A.; Churakov, G.; Berkes, P.; Arms, E.M.; Kelsey, D.; Brosius, J.; Kriegs, J.O.; Schmitz, J. Retroposon insertion patterns of neoavian birds: Strong evidence for an extensive incomplete lineage sorting era. Mol. Biol. Evol. 2012, 29, 1497–1501, doi:10.1093/molbev/msr319.
[62]  Haddrath, O.; Baker, A.J. Multiple nuclear genes and retroposons support vicariance and dispersal of the palaeognaths, and an Early Cretaceous origin of modern birds. Proc. R. Soc. B 2012, 279, 4617–4625, doi:10.1098/rspb.2012.1630.
[63]  Van Tuinen, M.; Butvill, D.B.; Kirsch, J.A.; Hedges, S.B. Convergence and divergence in the evolution of aquatic birds. Proc. R. Soc. B 2001, 268, 1345–1350.
[64]  McCormack, J.E.; Harvey, M.G.; Faircloth, B.C.; Crawford, N.G.; Glenn, T.C.; Brumfield, R.T. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS One 2013, 8, e54848.
[65]  Wetmore, A. A Classification for the Birds of the World; Smithsonian Institution: Washington, DC, USA, 1960; Volume 139, pp. 1–37.
[66]  Ericson, P.G.P. Evolution of terrestrial birds in three continents: Biogeography and parallel radiations. J. Biogeogr. 2012, 39, 813–824, doi:10.1111/j.1365-2699.2011.02650.x.
[67]  Mayr, G. Phylogenetic relationships of the paraphyletic “caprimulgiform” birds (nightjars and allies). J. Zool. Syst. Evol. Res. 2010, 48, 126–137.
[68]  Mayr, G. Metaves, Mirandornithes, Strisores and other novelties—A critical review of the higher-level phylogeny of neornithine birds. J. Zool. Syst. Evol. Res. 2011, 49, 58–76, doi:10.1111/j.1439-0469.2010.00586.x.
[69]  Cracraft, J.; Barker, F.K.; Braun, M.; Harshman, J.; Dyke, G.J.; Feinstein, J.; Stanley, S.; Cibois, A.; Schikler, P.; Beresford, P.; et al. Phylogenetic relationships among modern birds (Neornithes): Towards an avian tree of life. In Assembling the Tree of Life; Cracraft, J., Donoghue, M., Eds.; Oxford University Press: Oxford, UK, 2004; pp. 468–489.
[70]  Sangster, G. A name for the clade formed by owlet-nightjars, swifts and hummingbirds (Aves). Zootaxa 2005, 799, 1–6.
[71]  Sangster, G. A name for the flamingo-grebe clade. Ibis 2005, 147, 612–615.
[72]  Groth, J.G.; Barrowclough, G.F. Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Mol. Phylogenet. Evol. 1999, 12, 115–123, doi:10.1006/mpev.1998.0603.
[73]  Chubb, A.L. New nuclear evidence for the oldest divergence among neognath birds: The phylogenetic utility of ZENK (i). Mol. Phylogenet. Evol. 2004, 30, 140–151, doi:10.1016/S1055-7903(03)00159-3.
[74]  Barrowclough, G.F.; Groth, J.G.; Mertz, L.A. The RAG-1 exon in the avian order Caprimulgiformes: Phylogeny, heterozygosity, and base composition. Mol. Phylogenet. Evol. 2006, 41, 238–248.
[75]  Ericson, P.G.P.; Anderson, C.L.; Britton, T.; Elzanowski, A.; Johansson, U.S.; K?llersj?, M.; Ohlson, J.I.; Parsons, T.J.; Zuccon, D.; Mayr, G. Diversification of Neoaves: Integration of molecular sequence data and fossils. Biol. Lett. 2006, 2, 543–547.
[76]  Mindell, D.P.; Sorenson, M.D.; Huddleston, C.J.; Miranda, H.C., Jr.; Knight, A.; Sawchuk, S.J.; Yuri, T. Phylogenetic relationships among and within select avian orders based on mitochondrial DNA. In Avian Molecular Evolution and Systematics; Mindell, D.P., Ed.; Academic Press: San Diego, CA, USA, 1997; pp. 214–247.
[77]  Poe, S.; Chubb, A.L. Birds in a bush: Five genes indicate explosive evolution of avian orders. Evolution 2004, 58, 404–415.
[78]  Hardison, R.C.; Roskin, K.M.; Yang, S.; Diekhans, M.; Kent, W.J.; Weber, R.; Elnitski, L.; Li, J.; O'Connor, M.; Kolbe, D.; et al. Covariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution. Genome Res. 2003, 13, 13–26, doi:10.1101/gr.844103.
[79]  Tuffley, C.; Steel, M. Links between maximum likelihood and maximum parsimony under a simple model of site substitution. Bull. Math. Biol. 1997, 59, 581–607, doi:10.1007/BF02459467.
[80]  Holder, M.T.; Lewis, P.O.; Swofford, D.L. The Akaike information criterion will not choose the no common mechanism model. Syst. Biol. 2010, 59, 477–485, doi:10.1093/sysbio/syq028.
[81]  Huelsenbeck, J.P.; Alfaro, M.E.; Suchard, M.A. Biologically inspired phylogenetic models strongly outperform the No Common Mechanism model. Syst. Biol. 2011, 60, 225–232, doi:10.1093/sysbio/syq089.
[82]  Goloboff, P.A. Parsimony, likelihood, and simplicity. Cladistics 2003, 19, 91–103, doi:10.1111/j.1096-0031.2003.tb00297.x.
[83]  Cox, W.A.; Kimball, R.T.; Braun, E.L. Phylogenetic position of the New World quail (Odontophoridae): Eight nuclear loci and three mitochondrial regions contradict morphology and the Sibley-Ahlquist tapestry. Auk 2007, 124, 71–84, doi:10.1642/0004-8038(2007)124[71:PPOTNW]2.0.CO;2.
[84]  Crowe, T.M.; Bowie, R.C.K.; Bloomer, P.; Mandiwana, T.G.; Hedderson, T.A.J.; Randi, E.; Pereira, S.L.; Wakeling, J. Phylogenetics, biogeography and classification of, and character evolution in, gamebirds (Aves: Galliformes): Effects of character exclusion, data partitioning and missing data. Cladistics 2006, 22, 495–532, doi:10.1111/j.1096-0031.2006.00120.x.
[85]  Wenzel, J.W.; Siddall, M.E. Noise. Cladistics 1999, 15, 51–64, doi:10.1111/j.1096-0031.1999.tb00394.x.
[86]  Han, K.-L.; Robbins, M.B.; Braun, M.J. A multi-gene estimate of phylogeny in the nightjars and nighthawks (Caprimulgidae). Mol. Phylogenet. Evol. 2010, 55, 443–453, doi:10.1016/j.ympev.2010.01.023.
[87]  Robinson, D.F.; Foulds, L.R. Comparison of phylogenetic trees. Math. Biosci. 1981, 53, 131–147.
[88]  Farris, J.S. The retention index and the rescaled consistency index. Cladistics 1989, 5, 417–419, doi:10.1111/j.1096-0031.1989.tb00573.x.
[89]  Livezey, B.C.; Zusi, R.L. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy: II.—Analysis and discussion. Zool. J. Linn. Soc. 2007, 149, 1–94, doi:10.1111/j.1096-3642.2006.00293.x.
[90]  Clarke, J.A.; Ksepka, D.T.; Smith, N.A.; Norell, M.A. Combined phylogenetic analysis of a new North American fossil species confirms widespread Eocene distribution for stem rollers (Aves, Coracii). Zool. J. Linn. Soc. 2009, 157, 586–611.
[91]  Mayr, G.; Mourer-Chauviré, C.; Weidig, I. Osteology and systematic position of the Eocene Primobucconidae (Aves, Coraciiformes sensu stricto), with first records from Europe. J. Syst. Paleontol. 2004, 2, 1–12, doi:10.1017/S1477201903001093.
[92]  Kriegs, J.O.; Matzke, A.; Churakov, G.; Kuritzin, A.; Mayr, G.; Brosius, J.; Schmitz, J. Waves of genomic hitchhikers shed light on the evolution of gamebirds (Aves: Galliformes). BMC Evol. Biol. 2007, 7, 190.
[93]  Sullivan, J.; Swofford, D.L. Should we use model-based methods for phylogenetic inference when we know assumptions about among-site rate variation and nucleotide substitution pattern are violated? Syst. Biol. 2001, 50, 723–729, doi:10.1080/106351501753328848.
[94]  Johnson, K.P. Deletion bias in avian introns over evolutionary timescales. Mol. Biol. Evol. 2004, 21, 599–602, doi:10.1093/molbev/msh051.
[95]  Alekseyenko, A.V.; Lee, C.J.; Suchard, M.A. Wagner and Dollo: A stochastic duet by composing two parsimonious solos. Syst. Biol. 2008, 57, 772–784.
[96]  Maddison, W.P. Gene trees in species trees. Syst. Biol. 1997, 46, 523–536, doi:10.1093/sysbio/46.3.523.
[97]  Oliver, J.C. Microevolutionary processes generate phylogenomic discordance at ancient divergences. Evolution 2013, doi:10.1111/evo.12047.
[98]  Edwards, S.V. Is a new and general theory of molecular systematics emerging? Evolution 2009, 63, 1–19, doi:10.1111/j.1558-5646.2008.00549.x.
[99]  Cracraft, J. Avian higher-level relationships and classification: Nonpasseriforms. In The Howard and Moore Complete Checklist of the Birds of the World, 4th; Dickinson, E.C., Remsen, J.V., Eds.; Aves Press: Northhampton, UK, 2013; Volume 1. Non-passerines, in press.

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