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Evolution of the primate cytochrome c oxidase subunit II gene

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Abstract

We examined the nucleotide and amino acid sequence variation of the cytochrome c oxidase subunit II (COII) gene from 25 primates (4 hominoids, 8 Old World monkeys, 2 New World monkeys, 2 tarsiers, 7 lemuriforms, 2 lorisiforms). Marginal support was found for three phylogenetic conclusions: (1) sister-group relationship between tarsiers and a monkey/ape clade, (2) placement of the aye-aye (Daubentonia) sister to all other strepsirhine primates, and (3) rejection of a sister-group relationship of dwarf lemurs (i.e., Cheirogaleus) with lorisiform primates. Stronger support was found for a sister-group relationship between the ring-tail lemur (Lemur catta) and the gentle lemurs (Hapalemur). In congruence with previous studies on COII, we found that the monkeys and apes have undergone a nearly two-fold increase in the rate of amino acid replacement relative to other primates. Although functionally important amino acids are generally conserved among all primates, the acceleration in amino acid replacements in higher primates is associated with increased variation in the amino terminal end of the protein. Additionally, the replacement of two carboxyl-bearing residues (glutamate and aspartate) at positions 114 and 115 may provide a partial explanation for the poor enzyme kinetics in cross-reactions between the cytochromes c and cytochrome c oxidases of higher primates and other mammals.

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References

  • Adkins RM, Honeycutt RL (In press) A molecular examination of archontan and chiropteran monophyly. Ad Primatol

  • Adkins RM, Honeycutt RL (1991) Molecular phylogeny of the superorder Archonta. Proc Natl Acad Sci USA 88:10317–10321

    Google Scholar 

  • Ammerman LK, Hillis DM (1992) A molecular test of bat relationships: monophyly or diphyly? Syst Biol 41:222–232

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Baba ML, Darga LL, Goodman M, Czelusniak J (1981) Evolution of cytochrome c investigated by the maximum parsimony method. J Mol Evol 17:197–213

    Google Scholar 

  • Bailey WJ, Slightom JL, Goodman M (1992a) Rejection of the “flying primate” hypothesis by phylogenetic evidence from the betaglobin gene. Science 256:86–89

    Google Scholar 

  • Bailey WJ, Hayasaka K, Skinner CG, Kehoe S, Sieu LC, Slightom JL, Goodman M (1992b) Reexamination of the African hominoid trichotomy with additional sequences from the primate beta-globin gene cluster. Mol Phylo Evol 1:97–135

    Google Scholar 

  • Bonner TI, Heinemann R, Todaro GJ (1980) Evolution of DNA sequences has been retarded in Malagasy primates. Nature 286:420–423

    Google Scholar 

  • Brown GG, Simpson MV (1982) Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci 79:3246–3250

    Google Scholar 

  • Brown WM (1985) The mitochondrial genome of animals. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 95–130

    Google Scholar 

  • 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

    Google Scholar 

  • Cann RL, Brown WM, Wilson AC (1984) Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics 106:479–499

    Google Scholar 

  • Capaldi RA (1990) Structure and function of cytochrome c oxidase. Annu Rev Biochem 59:569–596

    Google Scholar 

  • Capaldi RA, Malatesta F, Darley-Usmar VM (1983) Structure of cytochrome c oxidase. Biochem Biophys Acta 726:135–148

    Google Scholar 

  • Dene H, Goodman M, Prychodko W (1976) Immunodiffusion evidence on the phylogeny of the primates. In: Goodman M, Tashian RE (eds) Molecular anthopology. Plenum, New York, pp 171–195

    Google Scholar 

  • Dene H, Goodman M, Prychodko W (1980) Immunodiffusion systematics of the Primates. IV. Lemuriformes. Mammalia 44:211–223

    Google Scholar 

  • Disotell TR, Honeycutt RL, Ruvolo M (1992) Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini. Mol Biol Evol 9:1–13

    Google Scholar 

  • Dutrillaux B, Rumpler Y (1988) Absence of chromosomal similarities between tarsiers (Tarsius syrichta) and other primates. Folia Primatol 50:130–133

    Google Scholar 

  • Farris JS (1989) The retention index and resealed consistency index. Cladistics 5:417–419

    Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1992) PHYLIP: phylogenetic interference package, version 3.4. Program and documentation. Department of Genetics, University of Washington, Seattle, WA

    Google Scholar 

  • Ferris SD, Wilson AC, Brown WM (1981) Evolutionary tree for apes and humans based on cleavage maps of mitochondrial DNA. Proc Natl Acad Sci USA 78:2432–2436

    Google Scholar 

  • Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Molec Biol 37:105–164

    Google Scholar 

  • Gregory WK (1915) I. On the relationship of the Eocene lemur Notharctus to the Adapidae and to other primates. II. On the classification and phylogeny of the Lemuroidea. Bull Geol Soc Am 26:419–446

    Google Scholar 

  • Groves CP (1974) Taxonomy and phylogeny of prosimians. In: Martin RD, Doyle GA, Walker AC (eds) Prosimian biology. Duckworth, London, pp 435–448

    Google Scholar 

  • Groves CP (1989) A theory of human and primate evolution. Clarendon Press, Oxford

    Google Scholar 

  • Groves CP, Eaglen RH (1988) Systematics of the Lemuridae (Primates, Strepsirhini). J Hum Evol 17:513–538

    Google Scholar 

  • Harrison T (1987) The phyletic relationships of the early catarrhine primates: a review of the current evidence. J Hum Evol 16:41–80

    Google Scholar 

  • Hasegawa M, Kishino H, Hayasaka K, Horai S (1990) Mitochondrial DNA evolution in Primates: transition rate has been extremely low in the lemur. J Mol Evol 31:113–121

    Google Scholar 

  • Hillis DM (1991) Discriminating between phylogenetic signal and random noise in DNA sequences. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 278–294

    Google Scholar 

  • Hillis DM, Huelsenbeck JP (1992) Signal, noise, and reliability in molecular phylogenetic analyses. J Hered 83:189–195

    Google Scholar 

  • Holmquist R (1983) Transitions and transversions in evolutionary descent: an approach to understanding. J Mol Evol 19:134–144

    Google Scholar 

  • Irwin DM, Koeher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Google Scholar 

  • Jung KY, Crovella S, Rumpler Y (1992) Phylogenetic relationships among lemuriform species determined from restriction genomic DNA banding patterns. Folia Primatol 58:224–229

    Google Scholar 

  • Keohavang P, Thilly WG (1989) Fidelity of DNA polymerase in DNA amplification. Proc Natl Acad Sci USA 86:9253–9257

    Google Scholar 

  • Koop BF, Tagle DA, Goodman M, Slightom JL (1989) A molecular view of primate phylogeny and important systematic and evolutionary questions. Mol Biol Evol 6:580–612

    Google Scholar 

  • Kraft R, Tardiff J, Krauter KS, Leinwand LA (1988) Using mini-prep plasmid DNA for sequencing double stranded templates with sequenase. Biotechniques 6:544–547

    Google Scholar 

  • Li W-H, Tanimura M (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326:93–96

    Google Scholar 

  • 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

    Google Scholar 

  • Li W-H, Guoy 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

    Google Scholar 

  • Liu H, Beckenbach AT (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol Phyl Evol 1:41–52

    Google Scholar 

  • Maniatis T, Fritch EF, Sambrook J (1982) Molecular cloning. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Mindell DP, Honeycutt RL (1990) Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annu Rev Ecol Syst 21:541–566

    CAS  Google Scholar 

  • Novacek MJ (1989) Higher mammal phylogeny: the morphological-molecular synthesis. In: Fernholm B, Bremer K, Jornvall H (eds) The hierarchy of life. Elsevier Science Publishers, BV, Amsterdam, pp 421–435

    Google Scholar 

  • Osheroff N, Speck SH, Margoliash E, Veerman ECI, Wilms J, König BW, Muijsers AO (1983) The reaction of primate cytochromes c with cytochrome c oxidase. J Biol Chem 258:5731–5738

    Google Scholar 

  • Pickford M (1986) The geochronology of Miocene higher primate faunas of East Africa. In: Else JG, Lee PC (eds) Primate evolution. Cambridge University Press, Cambridge, pp 19–33

    Google Scholar 

  • Ramharack R, Deeley RG (1987) Structure and evolution of primate cytochrome c oxidase subunit II gene. J Biol Chem 262:14014–14021

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schwartz E (1931) A revision of the genera and species of Madagascan Lemuridae. Proc Zool Soc Lond 1931:399–428

    Google Scholar 

  • Schwartz JH, Tattersall I (1985) Evolutionary relationships of living lemurs and lorises (Mammalia, Primates) and their potential affinities with European Eocene Adapidae. Anthropol Pap Am Mus Nat Hist 57:344–352

    Google Scholar 

  • Schwartz JH, Tattersall I (1987) Tarsiers, adapids and the integrity of Strepsirhini. J Hum Evol 16:23–40

    Google Scholar 

  • Seino S, Bell GI, Li W-H (1992) Sequences of primate insulin genes support the hypothesis of a slower rate of molecular evolution in humans and apes than in monkeys. Mol Biol Evol 9:193–203

    Google Scholar 

  • Simons EL, Rasmussen T (1989) Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade. Am J Phys Anthropol 79:1–23

    Google Scholar 

  • Simons EL, Rumpler Y (1988) Eulemur: new generic name for species of Lemur other than Lemur catta. CR Acad Sci Paris 307:547–551

    Google Scholar 

  • Stanhope MJ, Czelusniak J, Si J-S, Nickerson J, Goodman M (1992) A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein with convincing evidence for bat monophyly. Mol Phylo Evol 1:148–160

    Google Scholar 

  • Swofford DL (1990) PAUP: phylogenetic analysis using parsimony, version 3.0n. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Szalay FS, Katz CC (1973) Phylogeny of lemurs, galagos and lorises. Folia Primatol 19:88–103

    Google Scholar 

  • Tindall KR, Kunkel T (1988) Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry 27:6008–6013

    Google Scholar 

  • Williams SA, Goodman M (1989) A statistical test that supports a human/chimpanzee clade based on noncoding DNA sequence data. Mol Biol Evol 6:325–330

    Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–174

    CAS  PubMed  Google Scholar 

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  1. Department of Wildlife and Fisheries, Texas A&M University, 77843, College Station, TX, USA

    Ronald M. Adkins & Rodney L. Honeycutt

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  1. Ronald M. Adkins
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  2. Rodney L. Honeycutt
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Correspondence to: R.L. Honeycutt

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Adkins, R.M., Honeycutt, R.L. Evolution of the primate cytochrome c oxidase subunit II gene. J Mol Evol 38, 215–231 (1994). https://doi.org/10.1007/BF00176084

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