Abstract
The evolution of two mitochondrial genes, cytochrome b and cytochrome c oxidase subunit II, was examined in several eutherian mammal orders, with special emphasis on the orders Artiodactyla and Rodentia. When analyzed using both maximum parsimony, with either equal or unequal character weighting, and neighbor joining, neither gene performed with a high degree of consistency in terms of the phylogenetic hypotheses supported. The phylogenetic inconsistencies observed for both these genes may be the result of several factors including differences in the rate of nucleotide substitution among particular lineages (especially between orders), base composition bias, transition/transversion bias, differences in codon usage, and different constraints and levels of homoplasy associated with first, second, and third codon positions. We discuss the implications of these findings for the molecular systematics of mammals, especially as they relate to recent hypotheses concerning the polyphyly of the order Rodentia, relationships among the Artiodactyla, and various interordinal relationships.
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Adkins RM, Honeycutt RL (1991) Molecular phylogeny of the superorder Archonta. Proc Natl Acad Sci USA 88:10317–10321
Adkins RM, Honeycutt RL (1993) A molecular examination of archontan and chiropteran monophyly. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum Press, New York, pp 227–249
Adkins RM, Honeycutt RL (1994) Evolution of the primate cytochrome c oxidase II gene. J Mol Evol 38:215–231
Allard MW, Ellsworth DL, Honeycutt RL (1991a) The production of single-stranded DNA suitable for sequencing using the polymerase chain reaction. Biotechniques 10:24–26
Allard MW, Miyamoto MM, Honeycutt RL (1991b) Tests for rodent polyphyly. Nature 353:610–611
Allard MW, Honeycutt RL (1992) Nucleotide sequence variation in the mitochondrial 12S rRNA gene and the phylogeny of African molerats (Rodentia: Bathyergidae). Mol Biol Evol 9:27–40
Allard MW, Miyamoto MM, Jarecki L, Kraus F, Tennant MR (1992) DNA systematics and evolution of the artiodactyl family Bovidae. Proc Natl Acad Sci USA 89:3972–3976
Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Ro BA, Sange F, Schreie PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465
Anderson S, De Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717
Aquadro CF, Kaplan N, Risko KJ (1984) An analysis of the dynamics of mammalian mitochondrial DNA sequence evolution. Mol Biol Evol 1:423–434
Archie JW (1989) Homoplasy excess ratios: new indices for measuring levels of homoplasy in phylogenetic systematics and a critique of the consistency index. Syst Zool 38:253–269
Arnason U, 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
Arnason U, 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
Black CC (1963) A review of the North American Tertiary Sciuridae. Bull Mus Comp Zool Harvard 130:109–248
Bremer K (1988) The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803
Britten RJ (1986) Rates of DNA sequence evolution differ betweer taxonomic groups. Science 231:1393–1398
Brown WM (1980) Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. Proc Natl Acad Sci USA 77:3605–3609
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 USA 88:5974–5978
Carleton MD, Musser GG (1984) Muroid rodents. In: Anderson S, Jones JK (eds) Orders and families of recent mammals of the world. John Wiley & Son, New York, pp 289–379
Catzeflis FM, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Tree 7:122–126
Catzeflis FM, Dickerman AW, Michaux J, Kirsch JAW (1993) DNA hybridization and rodent phylogeny. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammalian phylogeny. Springer-Verlag, New York, pp 159–172
DeWalt TS, Sudman PD, Hafner MS, Davis SK (1993) Phylogenetic relationships of pocket gophers (Cratogeomys and Pappogeomys)_ based on mitochondrial DNA cytochrome b sequences. Mol Phyl Evol 2:193–204
Disotell TR, Honeycutt RL, Ruvolo M (1992) Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini. Mol Biol Evol 9:1–13
Eernisse DJ, Kluge AG (1993) Taxonomic congruence versus total evidence, and ammote phylogeny inferred from fossils, molecules, and morphology. Mol Biol Evol 10:1170–1195
Farris JS (1989) The retention index and resealed consistency index. Cladistics 5:417–419
Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Flynn LJ, Jacobs LL, Cheema IU (1986) Baluchimyinae, a new ctenodactyloid rodent subfamily from the Miocene of Baluchistan. Am Mus Novitates 2841:1–58
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
Gentry AW (1992) The subfamilies and tribes of the family Bovidae. Mammal Rev 22:1–32
Grant D (1993) Molecular phylogeny and the higher classification of eutherian mammals. Trends Ecol Evol 8:141–147
Grant D, Hide WA, Li W-H (1991) Is the guinea-pig a rodent? Nature 351:649–652
Grant D, Higgins DG (1994) Molecular evidence for the inclusion of cetaceans within the order Artiodactyla. Mol Biol Evol 11:357–364
Green M, Bjork PR (1980) On the genus Dikkomys (Geomyoidea, Mammalia). Palaeovertebrata, Montpellier, Mem Jubil R Lavocat: 343–353
Holmes ES (1991) Different rates of substitution may produce different phylogenies of the eutherian mammals. J Mol Evol 33:209–215
Honeycutt RL, Adkins RM (1993) Higher level systematics of eutherian mammals: an assessment of molecular characters and phylogenetic hypotheses. Annu Rev Ecol Syst 24:279–305
Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34
Irwin DM, Arnason U (1994) Cytochrome b gene of marine mammals: phylogeny and evolution. J Mamm Evol 2:37–55
Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144
Irwin DM, Wilson AC (1992) Limitations of molecular methods for establishing the phylogeny of mammals, with special reference to the position of elephants. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammalian phylogeny. Springer-Verlag, New York, pp 257–267
Janis CM, Scott KM (1987) The interrelationships of higher ruminant families with special emphasis on the members of the Cervoidea. Am Mus Novit 2893:1–85
Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Paabo, S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
Keohavang P, Thilly WG (1989) Fidelity of DNA polymerases in DNA amplification. Proc Natl Acad Sci USA 86:9253–9257
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25
Kraft R, Tardiff J, Kramer KS, Leinwand LA (1988) Using mini-prep plasmid DNA for sequencing double stranded templates with sequenase. Biotechniques 6:544–547
Kraus F, Miyamoto MM (1991) Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117–130
Kumar S, Tamura K, Nei M (1993) MEGA: molecular evolutionary genetics analysis, version 1.02. Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, Pennsylvania
Li W-H (1987) Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol 24:337–345
Li W-H, Hide WA, Zharkikh A, Ma D-P, Graur D (1992) The molecular taxonomy and evolution of the guinea pig. J Hered 83:174–181
Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342
Luckett WP, Hartenberger J-L (1985) Evolutionary relationships among rodents: a multidisciplinary analysis. Plenum Press, New York, pp 1–721
Luckett WP, Hartenberger J-L (1993) Monophyly or polyphyly of the order Rodentia: possible conflict between morphological and molecular interpretations. J Mammal Evol 1:127–147
Ma D-P, Zharkikh A, Grant D, VandeBerg JL, Li W-H (1993) Structure and evolution of opossum, guinea pig, and porcupine cytochrome b genes. J Mol Evol 36:327–334
Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90:4087–4091
Mindell DP, Honeycutt RL (1990) Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annu Rev Ecol Syst 21: 541–566
Miyamoto MM, Allard MW, Adkins RM, Janecek LL, Honeycutt RL (1994) A congruence test of reliability using linked mitochondrial DNA sequences. Syst Biol 43:236–249
Miyamoto MM, Kraus F, Laipis PJ, Tanhauser SM, Webb SD (1993) Mitochondrial DNA phylogenies within Artiodactyla. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammalian phylogeny. Springer-Verlag, New York, pp 268–281
Miyamoto MM, Kraus F, Ryder OA (1990) Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc Natl Acad Sci USA 87:6127–6131
Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125
O'hUigin C, Li W-H (1992) The molecular clock ticks regularly in muroid rodents and hamsters. J Mol Evol 35:377–384
Pesole G, Sbisa E, Mignotte F, Saccone C (1991) The branching order of mammals: phylogenetic trees inferred from nuclear and mitochondrial molecular data. J Mol Evol 33:537–542
Pilgrim GE (1947) The evolution of the buffaloes, oxen, sheep, and goats. J Linnean Soc London (Zoology) 41:272–286
Pumo DE, Phillips CJ, Barcia M, Millan C (1992) Three patterns of mitochondrial DNA nucleotide divergence in the meadow vole, Microtus pennsylvanicus. J Mol Evol 34:163–174
Russell RJ (1968a) Evolution and classification of the pocket gophers of the subfamily Geomyinae. Univ Kansas Pub Mus Nat Hist 16: 473–597
Russell RJ (1968b) Revision of pocket gophers of the genus Pappogeomys. Univ Kansas Pub Mus Nat Hist 16:581–776
Ruvolo M, Disotell TR, Allard MW, Brown WM, Honeycutt RL (1991) Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc Natl Acad Sci USA 88:1570–1574
Saiki RK, Gelfand DH, Stoeffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Savage DE, Russell DE (1983) Mammalian paleofaunas of the world. Addison-Wesley, Reading, MA
Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 16:8207–8211
Shields DC (1990) Switches in species-specific codon preferences: the influence of mutation biases. J Mol Evol 31:71–80
Sidow A, Wilson AC (1991) Compositional statistics evaluated by computer simulations. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 129–146
Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, version 3.1. Illinois Natural History Survey, Champaign, Illinois
Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285
Tamura K, Nei M (1993) Model selection in the estimation of the number of nucleotide substitutions. Mol Biol Evol 10:512–526
Thomas WK, Martin SL (1993) A recent origin of marmots. Mol Phyl Evol 2:330–336
Tindall KR, Kunkel TA (1988) Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry 27:6008–6013
Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitutions in rodents than in man. Proc Natl Acad Sci USA 82: 1741–1745
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Honeycutt, R.L., Nedbal, M.A., Adkins, R.M. et al. Mammalian mitochondrial DNA evolution: A comparison of the cytochrome b and cytochrome c oxidase II genes. J Mol Evol 40, 260–272 (1995). https://doi.org/10.1007/BF00163231
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DOI: https://doi.org/10.1007/BF00163231