Evidence from Nuclear DNA Sequences Sheds Light on the Phylogenetic Relationships of Pinnipedia: Single Origin with Affinity to Musteloidea

Abstract Considerable long-standing controversy and confusion surround the phylogenetic affinities of pinnipeds, the largely marine group of “fin-footed” members of the placental mammalian order Carnivora. Until most recently, the two major competing hypotheses were that the pinnipeds have a single (monophyletic) origin from a bear-like ancestor, or that they have a dual (diphyletic) origin, with sea lions (Otariidae) derived from a bear-like ancestor, and seals (Phocidae) derived from an otter-, mustelid-, or musteloid-like ancestor. We examined phylogenetic relationships among 29 species of arctoid carnivorans using a concatenated sequence of 3228 bp from three nuclear loci (apolipoprotein B, APOB; interphotoreceptor retinoid-binding protein, IRBP; recombination-activating gene 1, RAG1). The species represented Pinnipedia (Otariidae: Callorhinus, Eumetopias; Phocidae: Phoca), bears (Ursidae: Ursus, Melursus), and Musteloidea (Mustelidae: Mustela, Enhydra, Melogale, Martes, Gulo, Meles; Procyonidae: Procyon; Ailuridae: Ailurus; Mephitidae: Mephitis). Maximum parsimony, maximum likelihood, and Bayesian inference phylogenetic analyses of separate and combined datasets produced trees with largely congruent topologies. The analyses of the combined dataset resulted in well-resolved and well-supported phylogeny reconstructions. Evidence from nuclear DNA evolution presented here contradicts the two major hypotheses of pinniped relationships and strongly suggests a single origin of the pinnipeds from an arctoid ancestor shared with Musteloidea to the exclusion of Ursidae.

[1]  M. Goodman Macromolecular Sequences in Systematic and Evolutionary Biology , 2012, Monographs in Evolutionary Biology.

[2]  Ú. Árnason Localization of nucleolar organizing regions in pinniped karyotypes. , 2009, Hereditas.

[3]  Ú. Árnason The relationship between the four principal pinniped karyotypes. , 2009, Hereditas.

[4]  Ú. Árnason Comparative chromosome studies in Pinnipedia. , 2009, Hereditas.

[5]  C. Strobeck,et al.  A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. , 2005, Molecular phylogenetics and evolution.

[6]  Ziheng Yang,et al.  Branch-length prior influences Bayesian posterior probability of phylogeny. , 2005, Systematic biology.

[7]  J. J. Flynn,et al.  Molecular phylogeny of the carnivora (mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. , 2005, Systematic biology.

[8]  B. Rannala,et al.  Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. , 2004, Systematic biology.

[9]  O. Ryder,et al.  Phylogenetic relationships within mammalian order Carnivora indicated by sequences of two nuclear DNA genes. , 2004, Molecular phylogenetics and evolution.

[10]  I. Stirling,et al.  A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. , 2004, Molecular phylogenetics and evolution.

[11]  A. Hipp,et al.  Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. , 2004, Systematic biology.

[12]  J. Sato,et al.  Molecular Phylogeny of Arctoids (Mammalia: Carnivora) with Emphasis on Phylogenetic and Taxonomic Positions of the Ferret-badgers and Skunks , 2004, Zoological science.

[13]  O. Bininda-Emonds,et al.  Novel versus unsupported clades: assessing the qualitative support for clades in MRP supertrees. , 2003, Systematic biology.

[14]  A. Berta,et al.  Chapter 3 , 2003 .

[15]  T. Britton,et al.  Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. , 2003, Systematic biology.

[16]  R. Wayne,et al.  Type I STS markers are more informative than cytochrome B in phylogenetic reconstruction of the Mustelidae (Mammalia: Carnivora). , 2003, Systematic biology.

[17]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[18]  Antonis Rokas,et al.  Comparing bootstrap and posterior probability values in the four-taxon case. , 2003, Systematic biology.

[19]  Klaus-Peter Koepfli,et al.  A new phylogenetic marker, apolipoprotein B, provides compelling evidence for eutherian relationships. , 2003, Molecular phylogenetics and evolution.

[20]  S. Holmes,et al.  Bootstrapping Phylogenetic Trees: Theory and Methods , 2003 .

[21]  M. S. Lee,et al.  Partitioned likelihood support and the evaluation of data set conflict. , 2003, Systematic biology.

[22]  W. Doolittle,et al.  Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. , 2003, Molecular biology and evolution.

[23]  J. Sato,et al.  Phylogenetic Relationships and Divergence Times among Mustelids (Mammalia: Carnivora) Based on Nucleotide Sequences of the Nuclear Interphotoreceptor Retinoid Binding Protein and Mitochondrial Cytochrome b Genes , 2003, Zoological science.

[24]  F. Lutzoni,et al.  Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. , 2003, Molecular biology and evolution.

[25]  Masatoshi Nei,et al.  Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Derrick J. Zwickl,et al.  Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. , 2002, Molecular phylogenetics and evolution.

[27]  A. Janke,et al.  Mitogenomic analyses of eutherian relationships , 2002, Cytogenetic and Genome Research.

[28]  D. Yeates,et al.  Partitioned Bremer support and multiple trees , 2002, Cladistics : the international journal of the Willi Hennig Society.

[29]  J. Huelsenbeck,et al.  Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference , 2002, Bioinform..

[30]  F. K. Barker,et al.  The utility of the incongruence length difference test. , 2002, Systematic biology.

[31]  A. Janke,et al.  Mammalian mitogenomic relationships and the root of the eutherian tree , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. Lecointre,et al.  When does the incongruence length difference test fail? , 2002, Molecular biology and evolution.

[33]  C. Strobeck,et al.  Conserved primers for rapid sequencing of the complete mitochondrial genome from carnivores, applied to three species of bears. , 2002, Molecular biology and evolution.

[34]  R. Debry Improving interpretation of the decay index for DNA sequence data. , 2001, Systematic biology.

[35]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[36]  C. Matthee,et al.  Mining the mammalian genome for artiodactyl systematics. , 2001, Systematic biology.

[37]  B. Payseur,et al.  Failure of the ILD to determine data combinability for slow loris phylogeny. , 2001, Systematic biology.

[38]  Heather M. Amrine,et al.  Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction. , 2001, Molecular biology and evolution.

[39]  R. DeSalle,et al.  Phylogenetic utility of different types of molecular data used to infer evolutionary relationships among stalk-eyed flies (Diopsidae). , 2001, Systematic biology.

[40]  C. Orme,et al.  Noise and incongruence: interpreting results of the incongruence length difference test. , 2000, Molecular phylogenetics and evolution.

[41]  M. S. Lee,et al.  Tree robustness and clade significance. , 2000, Systematic biology.

[42]  J. J. Flynn,et al.  Whence the red panda? , 2000, Molecular phylogenetics and evolution.

[43]  Liang-kong Lin,et al.  Evolutionary trends of the mitochondrial lineage differentiation in species of genera Martes and Mustela. , 2000, Genes & genetic systems.

[44]  O. Bininda-Emonds,et al.  Factors influencing phylogenetic inference: a case study using the mammalian carnivores. , 2000, Molecular phylogenetics and evolution.

[45]  W. Moore,et al.  Comparative evolution of the mitochondrial cytochrome b gene and nuclear beta-fibrinogen intron 7 in woodpeckers. , 2000, Molecular biology and evolution.

[46]  R. Masuda,et al.  Intrageneric Diversity of the Cytochrome b Gene and Phylogeny of Eurasian Species of the Genus Mustela (Mustelidae, Carnivora) , 2000, Zoological science.

[47]  S. O’Brien,et al.  Patterns of diversity among SINE elements isolated from three Y-chromosome genes in carnivores. , 2000, Molecular biology and evolution.

[48]  N. Takezaki,et al.  A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. , 2000, Molecular phylogenetics and evolution.

[49]  Hitoshi Suzuki,et al.  A Phylogenetic View on Species Radiation in Apodemus Inferred from Variation of Nuclear and Mitochondrial Genes , 2000, Biochemical Genetics.

[50]  Diana J. Kao,et al.  Molecular evidence regarding the origin of echolocation and flight in bats , 2000, Nature.

[51]  J. Sumich,et al.  Marine Mammals: Evolutionary Biology , 1999 .

[52]  R. Baker,et al.  Corroboration among Data Sets in Simultaneous Analysis: Hidden Support for Phylogenetic Relationships among Higher Level Artiodactyl Taxa , 1999, Cladistics : the international journal of the Willi Hennig Society.

[53]  C. W. Kilpatrick,et al.  Phylogenetic Relationships of the Order Insectivora Based on Complete 12S rRNA Sequences from Mitochondria , 1999, Cladistics : the international journal of the Willi Hennig Society.

[54]  R. Masuda,et al.  Intraspecific Variation of Mitochondrial Cytochrome b Gene Sequences of the Japanese Marten Martes melampus and the Sable Martes zibellina (Mustelidae, Carnivora, Mammalia) in Japan , 1999 .

[55]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[56]  J. L. Gittleman,et al.  Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia) , 1999, Biological reviews of the Cambridge Philosophical Society.

[57]  M A Newton,et al.  Bayesian Phylogenetic Inference via Markov Chain Monte Carlo Methods , 1999, Biometrics.

[58]  R. Wayne,et al.  Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial cytochrome b sequences , 1998 .

[59]  K. Bauer,et al.  Immunogenetic Evidence for the Phylogenetic Sister Group Relationship of Dogs and Bears (Mammalia, Carnivora: Canidae and Ursidae) , 1998, Experimental and Clinical Immunogenetics.

[60]  F. Galibert,et al.  Traced orthologous amplified sequence tags (TOASTs) and mammalian comparative maps , 1998, Mammalian Genome.

[61]  G. Lecointre,et al.  The 'evolutionary signal' of homoplasy in protein-coding gene sequences and its consequences for a priori weighting in phylogeny. , 1998, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[62]  J. J. Flynn,et al.  Phylogeny of the Carnivora (Mammalia): congruence vs incompatibility among multiple data sets. , 1998, Molecular phylogenetics and evolution.

[63]  L. Barnes Evolution and adaptation of marine mammals in the pacific rim , 1997 .

[64]  R DeSalle,et al.  Multiple sources of character information and the phylogeny of Hawaiian drosophilids. , 1997, Systematic biology.

[65]  B. Rannala,et al.  Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method. , 1997, Molecular biology and evolution.

[66]  R. Woodroff Carnivore behavior, ecology, and evolution, vol. 2: Edited by John L. Gittleman Cornell University Press, 1996. £66.50 hbk, £29.50 pbk (xii + 644 pages) ISBN 0 8014 2190 X , 1997 .

[67]  R. Honeycutt,et al.  Systematics of Mustelid-Like Carnivores , 1997 .

[68]  M. Newton,et al.  Phylogenetic Inference for Binary Data on Dendograms Using Markov Chain Monte Carlo , 1997 .

[69]  Ú. Árnason,et al.  Phylogenetic relationships within caniform carnivores based on analyses of the mitochondrial 12S rRNA gene , 1996, Journal of Molecular Evolution.

[70]  B. Efron,et al.  Bootstrap confidence levels for phylogenetic trees. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  B. Efron,et al.  Bootstrap confidence levels for phylogenetic trees. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[72]  H. Takei,et al.  Amino acid sequences of hemoglobin β chains of five species of pinnipeds:Neophoca cinerea, Otaria byronia, Eumetopias jubatus, Pusa hispida, andPagophilus groenlandica , 1996, Journal of protein chemistry.

[73]  B. Rannala,et al.  Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference , 1996, Journal of Molecular Evolution.

[74]  Olivier Gascuel,et al.  On the Interpretation of Bootstrap Trees: Appropriate Threshold of Clade Selection and Induced Gain , 1996 .

[75]  S. Talbot,et al.  A phylogeny of the bears (Ursidae) inferred from complete sequences of three mitochondrial genes. , 1996, Molecular phylogenetics and evolution.

[76]  Michael A. Newton,et al.  Bootstrapping phylogenies: Large deviations and dispersion effects , 1996 .

[77]  Ú. Árnason,et al.  Phylogenetic analyses of complete cytochromeb genes of the order Carnivora with particular emphasis on the Caniformia , 1996, Journal of Molecular Evolution.

[78]  Carol J. Bult,et al.  Constructing a Significance Test for Incongruence , 1995 .

[79]  A. Zharkikh,et al.  Estimation of confidence in phylogeny: the complete-and-partial bootstrap technique. , 1995, Molecular phylogenetics and evolution.

[80]  A. Zharkikh Estimation of evolutionary distances between nucleotide sequences , 1994, Journal of Molecular Evolution.

[81]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[82]  Wen-Hsiung Li,et al.  What is the Bootstrap Technique , 1994 .

[83]  K. Bremer,et al.  BRANCH SUPPORT AND TREE STABILITY , 1994 .

[84]  M. Yoshida,et al.  A molecular phylogeny of the family Mustelidae (Mammalia, Carnivora), based on comparison of mitochondrial cytochrome b nucleotide sequences. , 1994, Zoological science.

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

[86]  W. Wheeler,et al.  Higher level relationships of the arctoid Carnivora based on sequence data and "total evidence". , 1994, Molecular phylogenetics and evolution.

[87]  M. Wolsan Phylogeny and classification of early European Mustelida (Mammalia: Carnivora) , 1993 .

[88]  A. Queiroz For Consensus (Sometimes) , 1993 .

[89]  Joseph Felsenstein,et al.  Is there something wrong with the bootstrap on phylogenies? A reply to Hillis and Bull , 1993 .

[90]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[91]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[92]  E. Otaka,et al.  The giant panda is closer to a bear, judged by α- and β-hemoglobin sequences , 1993, Journal of Molecular Evolution.

[93]  A. Zharkikh,et al.  Statistical properties of bootstrap estimation of phylogenetic variability from nucleotide sequences. I. Four taxa with a molecular clock. , 1992, Molecular biology and evolution.

[94]  A. Zharkikh,et al.  Statistical properties of bootstrap estimation of phylogenetic variability from nucleotide sequences: II. Four taxa without a molecular clock , 1992, Journal of Molecular Evolution.

[95]  Ú. Árnason,et al.  The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina , 1992, Journal of Molecular Evolution.

[96]  M. Goodman,et al.  A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. , 1992, Molecular phylogenetics and evolution.

[97]  S. Hedges The number of replications needed for accurate estimation of the bootstrap P value in phylogenetic studies. , 1992, Molecular biology and evolution.

[98]  P. Goloboff HOMOPLASY AND THE CHOICE AMONG CLADOGRAMS , 1991, Cladistics : the international journal of the Willi Hennig Society.

[99]  A. Berta,et al.  Skeletal morphology and locomotor capabilities of the archaic pinniped Enaliarctos mealsi , 1990 .

[100]  S. Fong,et al.  Characterization and comparative structural features of the gene for human interstitial retinol-binding protein. , 1990, The Journal of biological chemistry.

[101]  David Baltimore,et al.  The V(D)J recombination activating gene, RAG-1 , 1989, Cell.

[102]  J. Farris THE RETENTION INDEX AND THE RESCALED CONSISTENCY INDEX , 1989, Cladistics : the international journal of the Willi Hennig Society.

[103]  A. Wyss FLIPPERS AND PINNIPED PHYLOGENY: HAS THE PROBLEM OF CONVERGENCE BEEN OVERRATED? , 1989 .

[104]  James W. Archie,et al.  Homoplasy Excess Ratios: New Indices for Measuring Levels of Homoplasy in Phylogenetic Systematics and a Critique of the Consistency Index , 1989 .

[105]  H. Kishino,et al.  Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea , 1989, Journal of Molecular Evolution.

[106]  J. L. Gittleman Carnivore Behavior, Ecology, and Evolution , 1989, Springer US.

[107]  A. Wyss,et al.  Skeleton of the Oldest Known Pinniped, Enaliarctos mealsi , 1989, Science.

[108]  L. Barnes A new enaliarctine pinniped from the Astoria Formation, Oregon, and a classification of the Otariidae (Mammalia: Carnivora) , 1989, Contributions in science.

[109]  A. Wyss Evidence from flipper structure for a single origin of pinnipeds , 1988, Nature.

[110]  J. J. Flynn Ancestry of sea mammals , 1988, Nature.

[111]  K. Bremer THE LIMITS OF AMINO ACID SEQUENCE DATA IN ANGIOSPERM PHYLOGENETIC RECONSTRUCTION , 1988, Evolution; international journal of organic evolution.

[112]  R. Mahley,et al.  DNA sequence of the human apolipoprotein B gene. , 1987, DNA.

[113]  M. Miyamoto,et al.  Hemoglobin of pandas: Phylogenetic relationships of carnivores as ascertained with protein sequence data , 1986, Naturwissenschaften.

[114]  Ú. Árnason,et al.  Pinniped phylogeny enlightened by molecular hybridizations using highly repetitive DNA , 1986 .

[115]  M. Miyamoto,et al.  Biomolecular Systematics of Eutherian Mammals: Phylogenetic Patterns and Classification , 1986 .

[116]  W. W. Jong Protein sequence evidence for monophyly of the carnivore families Procyonidae and Mustelidae. , 1986 .

[117]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[118]  J. Felsenstein Confidence Limits on Phylogenies With a Molecular Clock , 1985 .

[119]  W. D. de Jong,et al.  Primary structures of the alpha-crystallin A chains of twenty-eight mammalian species, chicken and frog. , 1984, European journal of biochemistry.

[120]  Ø. Wiig On the Relationship of Pinnipeds to Other Carnivores , 1983 .

[121]  A. R. Templeton,et al.  PHYLOGENETIC INFERENCE FROM RESTRICTION ENDONUCLEASE CLEAVAGE SITE MAPS WITH PARTICULAR REFERENCE TO THE EVOLUTION OF HUMANS AND THE APES , 1983, Evolution; international journal of organic evolution.

[122]  Allan C. Wilson,et al.  Construction of phylogenetic trees for proteins and nucleic acids: Empirical evaluation of alternative matrix methods , 1978, Journal of Molecular Evolution.

[123]  A. Friday,et al.  On the evolution of myoglobin. , 1978, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[124]  J. Farris Phylogenetic Analysis Under Dollo's Law , 1977 .

[125]  R. Tedford,et al.  Relationship of Pinnipeds to Other Carnivores (Mammalia) , 1976 .

[126]  C. A. Repenning Adaptive evolution of sea lions and walruses , 1976 .

[127]  C. Ray Geography of Phocid Evolution , 1976 .

[128]  S. Ridgway,et al.  Mammals of the sea : biology and medicine , 1973 .

[129]  J. Farris Estimating Phylogenetic Trees from Distance Matrices , 1972, The American Naturalist.

[130]  W. Fitch Toward Defining the Course of Evolution: Minimum Change for a Specific Tree Topology , 1971 .

[131]  J. Farris Methods for Computing Wagner Trees , 1970 .

[132]  U. Seal Carnivora systematics: a study of hemoglobins. , 1969, Comparative biochemistry and physiology.

[133]  V. Sarich Pinniped origins and the rate of evolution of carnivore albumins. , 1969, Systematic zoology.

[134]  J. Farris,et al.  Quantitative Phyletics and the Evolution of Anurans , 1969 .

[135]  E. Mitchell Controversy over Diphyly in Pinnipeds , 1967 .

[136]  L. Cavalli-Sforza,et al.  PHYLOGENETIC ANALYSIS: MODELS AND ESTIMATION PROCEDURES , 1967, Evolution; international journal of organic evolution.

[137]  E. Feltz,et al.  CYTOGENETIC COMPARISON OF SOME PINNIPEDS (MAMMALIA: EUTHERIA) , 1967 .

[138]  J. Ling Functional Significance of Sweat Glands and Sebaceous Glands in Seals , 1965, Nature.

[139]  R. Sokal,et al.  A METHOD FOR DEDUCING BRANCHING SEQUENCES IN PHYLOGENY , 1965 .

[140]  R. Thorne,et al.  Phenetic and Phylogenetic Classification , 1964, Nature.

[141]  I. McLAREN Are the Pinnipedia Biphyletic , 1960 .

[142]  C. A. Leone,et al.  Comparative Serology of Carnivores , 1956 .

[143]  J. Felsenstein Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[144]  H. Kishino,et al.  Dating of the human-ape splitting by a molecular clock of mitochondrial DNA , 2005, Journal of Molecular Evolution.

[145]  Mark P. Simmons,et al.  How meaningful are Bayesian support values? , 2004, Molecular biology and evolution.

[146]  Ú. Árnason,et al.  A molecular view of pinniped relationships with particular emphasis on the true seals , 2004, Journal of Molecular Evolution.

[147]  A. Austin,et al.  Increased congruence does not necessarily indicate increased phylogenetic accuracy--the behavior of the incongruence length difference test in mixed-model analyses. , 2002, Systematic biology.

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

[149]  D. A. Kramerov,et al.  CAN—a pan-carnivore SINE family , 2001, Mammalian Genome.

[150]  J. J. Flynn,et al.  Tempo and mode of evolution in an orthologous Can SINE , 2001, Mammalian Genome.

[151]  B. Larget,et al.  Markov Chain Monte Carlo Algorithms for the Bayesian Analysis of Phylogenetic Trees , 2000 .

[152]  R. Olmstead,et al.  A simulation study of reduced tree-search effort in bootstrap resampling analysis. , 2000, Systematic biology.

[153]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[154]  George Gaylord Simpson,et al.  Classification of mammals : above the species level , 1997 .

[155]  K. Lange Reconstruction of Evolutionary Trees , 1997 .

[156]  L. Werdelin Carnivoran ecomorphology: a phylogenetic perspective , 1996 .

[157]  D. Penny,et al.  Use of spectral analysis to test hypotheses on the origin of pinnipeds. , 1995, Molecular biology and evolution.

[158]  J. Leunissen,et al.  Eye Lens Crystallins and the Phylogeny of Placental Orders: Evidence for a Macroscelid-Paenungulate Clade , 1993 .

[159]  J. Sgouros,et al.  A Molecular View of Primate Supraordinal Relationships from the Analysis of Both Nucleotide and Amino Acid Sequences , 1993 .

[160]  John J. Flynn,et al.  A Phylogenetic Analysis and Definition of the Carnivora , 1993 .

[161]  Ú. Árnason,et al.  The Use of Highly Repetitive DNA for Resolving Cetacean and Pinniped Phylogenies , 1993 .

[162]  A. Berta New Enaliarctos (Pinnipedimorpha) from the Oligocene and Miocene of Oregon and the role of "Enaliarctids" in Pinniped phylogeny , 1991 .

[163]  M. Wolsan Pochodzenie i ewolucja ssaków morskich Polski , 1991 .

[164]  M. McKenna The alpha crystallin A chain of the eye lens and mammalian phylogeny , 1991 .

[165]  T. Nojima A MORPHOLOGICAL CONSIDERATION OF THE RELATIONSHIPS OF PINNIPEDS TO OTHER CARNIVORANS BASED ON THE BONY TENTORIUM AND BONY FALX , 1990 .

[166]  M. Goodman,et al.  Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of eutheria , 1990 .

[167]  W. C. Wozencraft The Phylogeny of the Recent Carnivora , 1989 .

[168]  S. O’Brien,et al.  Molecular and Biochemical Evolution of the Carnivora , 1989 .

[169]  J. Flynn Phylogeny of the Carnivora , 1988 .

[170]  G. Braunitzer,et al.  [Hemoglobins of pandas]. , 1987, Comptes rendus des seances de la Societe de biologie et de ses filiales.

[171]  A. Wyss The walrus auditory region and the monophyly of pinnipeds. American Museum novitates ; no. 2871 , 1987 .

[172]  J. Couturier,et al.  Evolution chromosomique chez les carnivores , 1986 .

[173]  D. Domning,et al.  STATUS OF STUDIES ON FOSSIL MARINE MAMMALS , 1985 .

[174]  L. Ginsburg Sur la position systématique du petit panda, Ailurus fulgens (Carnivora, Mammalia) , 1982 .

[175]  W. W. Jong Eye Lens Proteins and Vertebrate Phylogeny , 1982 .

[176]  C. Muizon Les relations phylogenetiques des Lutrinae (Mustelidae, Mammalia) , 1982 .

[177]  Morris Goodman,et al.  Mammalian phylogeny studied by sequence analysis of the eye lens protein alpha-crystallin , 1981 .

[178]  A. J. Gray,et al.  Paleobiogeography: Current Concerns. (Book Reviews: Historical Biogeography, Plate Tectonics, and the Changing Environment) , 1980 .

[179]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

[180]  E. Mitchell,et al.  The Enaliarctinae : a new group of extinct aquatic Carnivora and a consideration of the origin of the Otariidae. Bulletin of the AMNH ; v. 151, article 3 , 1973 .

[181]  N. I. Phillips,et al.  Carnivora systematics: immunological relationships of bear serum albumins. , 1970, Comparative biochemistry and physiology.

[182]  Maximilian Weber Die säugetiere. Einführung in die anatomie und systematik der recenten und fossilen Mammalia, von dr Max Weber. , 1904 .

[183]  Maximilian Weber Die Säugetiere : Einführung in die Anatomie und Systematik der recenten und fossilen Mammalia , 1904 .