Abstract
The phylogenetic relationships among Primates (human), Artiodactyla (cow), Cetacea (whale), Carnivora (seal), and Rodentia (mouse and rat) were estimated from the inferred amino acid sequences of the mitochondrial genomes using Marsupialia (opossum), Aves (chicken), and Amphibia (Xenopus) as an outgroup. The overall evidence of the maximum likelihood analysis suggests that Rodentia is an outgroup to the other four eutherian orders and that Cetacea and Artiodactyla form a clade with Carnivora as a sister taxon irrespective of the assumed model for amino acid substitutions. Although there remains an uncertainty concerning the relation among Artiodactyla, Cetacea, and Carnivora, the existence of a clade formed by these three orders and the outgroup status of Rodentia to the other eutherian orders seems to be firmly established. However, analyses of individual genes do not necessarily conform to this conclusion, and some of the genes reject the putatively correct tree with nearly 5% significance. Although this discrepancy can be due to convergent or parallel evolution in the specific genes, it was pointed out that, even without a particular reason, such a discrepancy can occur in 5% of the cases if the branching among the orders in question occurred within a short period. Due to uncertainty about the assumed model underlying the phylogenetic inference, this can occur even more frequently. This demonstrates the importance of analyzing enough sequences to avoid the danger of concluding an erroneous tree.
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References
Adachi J, Hasegawa M (1992a) Computer Science Monographs, No. 27. MOLPHY: Programs for Molecular Phylogenetics, I. —PROTML: Maximum Likelihood Inference of Protein Phylogeny. Institute of Statistical Mathematics, Tokyo
Adachi J, Hasegawa M (1992b) Amino acid substitution of proteins coded for in mitochondrial DNA during mammalian evolution. Jpn J Genet 67:187–197
Adachi J, Cao Y, Hasegawa M (1993) Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: rapid evolution in warm-blooded vertebrates. J Mol Evol 36:270–281
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Contr AC-19:716–723
Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith ALH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–464
Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) The complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717
Árnason Ú, Gullberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J Mol Evol 33:556–568
Árnason Ú, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34:493–505
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239
Bulmer M, Wolfe KH, Sharp PM (1991) Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci U S A 88:5974–5978
Czelusniak J, Goodman M, Koop BF, Tagle DA, Shoshani J, Braunitzer G, Kleinschmidt TK, de Jong WW, Matsuda G (1990) Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of Eutheria. In: Genoways HH (ed) Current mammalogy, vol 2. Plenum Press, New York, pp 545–572
Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington, DC, pp 345–352
Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome: a novel gene order in higher vertebrates. J Mol Biol 212:599–634
Easteal S (1990) The pattern of mammalian evolution and the relative rate of molecular evolution. Genetics 124:165–173
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1990) PHYLIP, Version 3.3. University Washington, Seattle
Fukami-Kobayashi K, Tateno Y (1991) Robustness of maximum likelihood tree estimation against different patterns of base substitutions. J Mol Evol 32:79–91
Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sbisa E, Saccone C (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516
Graur D (1993) Molecular phylogeny and the higher classification of eutherian mammals. Trends Ecol Evol 8:141–147
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hasegawa M, Cao Y, Adachi J, Yano T (1992) Rodent polyphyly? Nature 355:595–595
Hasegawa M, Fujiwara M (1993) Relative efficiencies of the maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phyl Evol 2:1–5
Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993) Early divergences in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388
Hasegawa M (1994) Inference of evolutionary trees from DNA and protein sequence data. In: Bozdogan H (ed) The frontiers of statistical modeling: an informational approach, vol 3. Engineering and Scientific Applications, Kluwer Academic Publ, Dordrecht, pp 241–248
Hasegawa M, Kishino H (1994) Accuracies of the simple methods for estimating the bootstrap probability of a maximum likelihood tree. Mol Biol Evol 11:142–145
Hashimoto T, Otaka E, Adachi J, Mizuta K, Hasegawa M (1993) The giant panda is most close to a bear, judged by α- and β-hemoglobin sequences. J Mol Evol 36:282–289
Hashimoto T, Nakamura Y, Nakamura F, Shirakura T, Adachi J, Goto N, Okamoto K, Hasegawa M (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol Biol Evol 11:65–71
Horai S, Satta Y, Hayasaka K, Kondo R, Inoue T, Ishida T, Hayashi S, Takahata N (1992) Man's place in Hominoidea revealed by mitochondrial DNA genealogy. J Mol Evol 35:32–43
Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Pääbo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosci 8:275–282
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179
Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160
Kojima S, Hashimoto T, Hasegawa M, Murata S, Ohta S, Seki H, Okada N (1993) Close phylogenetic relationship between Vestimentifera (tube worms) and Annelida revealed by the amino acid sequence of elongation factor-1α. J Mol Evol 37:66–70
Li W-H, Gouy M, Sharp PM, O'hUigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707
McKenna MC (1975) Toward a phylogenetic classification of the mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates: a multidisciplinary approach. Plenum Press, New York, pp 21–46
Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125
Roe BA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774
Romer AS (1966) Vertebrate paleontology. University of Chicago Press, Chicago
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. D Reidel Publ Comp, Dordrecht
Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85:1–350
Stewart C-B, Schilling JW, Wilson AC (1987) Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404
Wyss AR, Novacek MJ, McKenna MC (1987) Amino acid sequence versus morphological data and the interordinal relationships of mammals. Mol Biol Evol 4:99–116
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Cao, Y., Adachi, J., Janke, A. et al. Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: Instability of a tree based on a single gene. J Mol Evol 39, 519–527 (1994). https://doi.org/10.1007/BF00173421
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DOI: https://doi.org/10.1007/BF00173421