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The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: Sequence divergence in hymenoptera may be associated with nucleotide content

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Abstract

Polymerase chain reaction (PCR) followed by sequencing of single-stranded DNA yielded sequence information from the cytochrome b (cyt b) region in mitochondrial DNA from the ant Tetraponera rufoniger. Compared with the cyt b genes from Apis mellifera, Drosophila melanogaster, and D. yakuba, the overall A + T content (A + T%) of that of T. rufoniger is lower (69.9% vs 80.7%, 74.2%, and 73.9%, respectively) than those of the other three. The codon usage in the cyt b gene of T. rufoniger is biased although not as much as in A. mellifera, D. melanogaster, and D. yakuba; T. rufoniger has eight unused codons whereas D. melanogaster, D. yakuba, and A. mellifera have 21, 20, and 23, respectively. The inferred cyt b polypeptide chain (PPC) of T. rufoniger has diverged at least as much from a common ancestor with D. yakuba as has that of A. mellifera (∼3.5 vs ∼2.9). Despite the lower A + T%, the relative frequencies of amino acids in the cyt b PPC of T. rufoniger are significantly (P < 0.05) associated with the content of adenine and thymine (A + T%) and size of codon families. The mitochondrially located cytochrome oxidase subunit 11 genes (CO-II) of endopterygote insects have significantly higher average A + T% (∼75%) than those of exopterygous (∼69%o) and paleopterous (∼69%) insects. The increase in A + T% of endopterygote insects occurred in Upper Carboniferous and coincided with a significant acceleration of PPC divergence. However, acceleration of PPC divergence is not significantly correlated with the increase of the A + T% (P > 0.1). The high A + T%, the biased codon usage, and the increased PPC divergence of Hymenoptera can in that respect most easily be explained by directional mutation pressure which began in the Upper Carboniferous and still occurs in most members of the order. Given the roughly identical A + T% of the cyt b and CO-II genes from the other insects whose DNA sequences are known (A. mellifera, D. melanogaster, and D. yakuba), it seems most likely that the A + T% of T. rufoniger declined secondarily within the last 100 Myr as a result of a reduced directional mutation pressure.

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Abbreviations

Myr:

million years

mtDNA:

mitochondrial DNA

scnDNA:

single-copy nuclear DNA

A:

adenine

C:

cytosine

G:

guanine

T:

thymine

A + T%:

content of A and T

PPC:

polypeptide chain

cyt b :

cytochrome b

CO-I:

cytochrome oxidase sub-unit I

CO-II:

cytochrome oxidase subunit II

ND1:

NADH dehydrogenase subunit 1

ND6:

NADH dehydrogenase subunit 6

tRNA supSerinfUCN ucN:

transfer RNA for serine with a UCN anticodon

References

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulsen AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organisation of the human mitochondrial genome. Nature 290:457–465

    CAS  PubMed  Google Scholar 

  • Anderson S, de Bruijn MHL, Coulsen 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

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organisation of mouse mitochondrial DNA. Cell 26:167–180

    Google Scholar 

  • Birley AJ, Croft JH (1990) Mitochondrial DNAs and phylogenetic relationships. In: Dutta SK (ed) DNA systematics. CRC Press, Boca Raton, pp 107–137

    Google Scholar 

  • Bodmer M, Ashburner M (1984) Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species of Drosophila. Nature 300:425–427

    Google Scholar 

  • Boer PH, Hickey DA (1986) The alpha-amylase gene in Drosophila melanogaster: nucleotide sequence, gene structure and expression motifs. Nucleic Acids Res 14:46–55

    Google Scholar 

  • Brandão CRF (1990) Phylogenetic, biogeographic, and evolutionary inferences from the description of an early cretaceous South American Myrmeciinae. In: Veeresh GK, Mallik B, Viraktamath CA (eds) Social insects and the environment. Oxford and Ibh Publishing, New Delhi, pp 313–314

    Google Scholar 

  • Brandão CRF, Martins-Neto RG, Vulcano MA (1989) The earliest known fossil ant (first southern hemisphere mesozoic record) (Hymenoptera: Formicidae: Myrmeciinae). Psyche 96:195–208

    Google Scholar 

  • Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398

    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, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    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 

  • Cameron SA, Derr JN, Austin AD, Woolley JB, Wharton RA (1992) The application of nucleotide sequence data to phylogeny of the Hymenoptera: a review. J Hym Res 1:63–79

    Google Scholar 

  • Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization, and genetic code of mitochondrial genome of Paracentrotus lividus. J Biol Chem 264:10965–10975

    Google Scholar 

  • Carpenter FM, Burnham L (1985) The geological record of insects. Annu Rev Earth Planet Sci 13:297–314

    Google Scholar 

  • Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    Google Scholar 

  • Crozier RH (1990) From population genetics to phylogeny: uses and limits of mitochondrial DNA. Aust Syst Bot 3:111–124

    Google Scholar 

  • Crozier RH (1992) Molecular methods for insect phylogenetics. In: Whitten MJ, Oakeshott JG (eds) Molecular approaches to pure and applied entomology. Springer-Verlag, Berlin, pp 164–221

    Google Scholar 

  • Crozier RH, Crozier YC, Mackinley AG (1989) The CO-I and CO-II region of the honeybee mitochondrial DNA: evidence of variation in insect mitochondrial evolutionary rates. Mol Biol Evol 6: 399–411

    Google Scholar 

  • Crozier RH, Crozier YC (1992) The cytochrome b and ATPase genes of honeybee mitochondrial DNA. Mol Biol Evol 9:474–482

    Google Scholar 

  • Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 113:97–117

    Google Scholar 

  • Crozier YC, Koulianos S, Crozier RH (1991) An improved test for africanized honeybee mitochondrial DNA. Experientia 47:968–969

    Google Scholar 

  • de Bruijn MHL (1983) Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304:234–241

    Google Scholar 

  • Derr IN, Davis SK, Woolley JB, Wharton RA (1992a) Variation and the phylogenetic utility of the large ribosomal subunit of mitochondrial DNA from the insect order Hymenoptera. Mol Phyl Evol 1:136–147

    Google Scholar 

  • Derr JN, Davis SK, Woolley JB, Wharton RA (1992b) Reassessment of the 16S rRNA nucleotide sequence from members of the parasitic Hymenoptera. Mol Phyl Evol 1:338–341

    Google Scholar 

  • DeSalle R, Freedman T, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol 26:157–164

    Google Scholar 

  • Desjardin 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

    CAS  PubMed  Google Scholar 

  • di Rago J-P, Netter P, Slonimski PP (1990) Pseudo-wild type revertants from inactive apocytochrome b mutants as a tool for the analysis of the structure/function relationships of the mitochondrial ubiquinol-cytochrome c reductase of Saccharomyces cerevisiae. J Biol Chem 265:3332–3339

    Google Scholar 

  • Efron B, Gong G (1983) A leisurely look at the bootstrap, the jackknife and cross-validation. Am Stat 37:37–48

    Google Scholar 

  • Freese E (1962) On the evolution of base composition of DNA. J Theor Biol 3:82–101

    Google Scholar 

  • French S, Robson B (1983) What is a conservative substitution? J Mol Evol 19:171–175

    Google Scholar 

  • Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sbisà 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

    Google Scholar 

  • Garesse R (1988) Drosophila melanogaster mitochondrial DNA: gene organization and evolutionary considerations. Genetics 118:649–663

    Google Scholar 

  • Gillespie JH (1986) Variability of evolutionary rates of DNA. Genetics 113:1077–1091

    Google Scholar 

  • Harrison RG (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol Evol 4:6–11

    Google Scholar 

  • Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015–1069

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Honeycutt RL, Wheeler WC (1990) Mitochondrial DNA: variation in humans and higher primates. In: Dutta SK, Winter WP (eds) DNA systematics. CRC Press, Boca Raton, pp 91–129

    Google Scholar 

  • Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472

    Google Scholar 

  • Howell N (1989) Evolutionary conservation of protein regions in the protonmotive cytochrome b and their possible roles in redox catalysis. J Mol Evol 29:157–169

    Google Scholar 

  • Howell N, Gilbert K (1988) Mutational analysis of the mouse mitochondrial cytochrome b gene. J Mol Biol 203:607–618

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217

    Google Scholar 

  • Keith TP, Riley MA, Kreitman M, Lewontin RC, Curtis D, Chambers G (1987) Sequence of the structural gene for xanthine dehydrogenase (rosy locus) in Drosophila melanogaster. Genetics 116:67–73

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, pp 1–367

    Google Scholar 

  • Koulianos S, Crozier RH (1991) Two ancient mitochondrial alleles in Australian honeybees. Apidologie 22:621–626

    Google Scholar 

  • Kusmierski R, Borgia G, Crozier RH, Chan BHY (1993) Molecular information on bower-bird phylogeny and the evolution of exaggerated male characteristics. J Evol Biol 6:737–752

    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 

  • 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 

  • Meyer A, Wilson AC (1990) Origin of tetrapodes inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364

    Google Scholar 

  • Michener CD, Grimaldi DA (1988) The oldest fossil bee: apoid history, evolutionary stasis, and antiquity of social behaviour. Proc Natl Acad Sci USA 85:6424–6426

    Google Scholar 

  • Miyamoto MM, Boyle SM (1989) The potential importance of mitochondrial DNA sequence data to eutherian mammal phylogeny. In: Femholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Elsevier, Amsterdam, pp 437–450

    Google Scholar 

  • Miyata T, Hayashida H, Kikuno R, Hasagawa M, Kobayashi M, Koike K (1982) Molecular clock of silent substitution: at least sixfold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol 19:28–35

    Google Scholar 

  • Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Anon Rev Ecol Syst 18:269–292

    Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169

    Google Scholar 

  • Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498

    CAS  PubMed  Google Scholar 

  • Osawa S, Jukes TH, Watanabe K, Mum A (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264

    Google Scholar 

  • Powell JR, Caccone A, Amato GD, Yoon C (1986) Rates of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83:9090–9093

    Google Scholar 

  • Preparata G, Saccone C (1991) DNA markov clocks in gene evolution. Evol Biol 5:45–58

    Google Scholar 

  • Roe BA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial DNA. J Biol Chem 260:9759–9774

    Google Scholar 

  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Millis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. 2nd ed. Cold Spring Harbor Lab Press, Cold Spring Harbor

    Google Scholar 

  • Sander M, Lowenhaupt K, Rich A (1991) Drosophila Rrpl protein: an apurinic endonuclease with homologous recombination activities. Proc Natl Acad Sci USA 88:6780–6784

    Google Scholar 

  • Sanger F, Nicklen S, Coulsen AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd ed. Freeman, New York, pp 1–859

    Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592

    Google Scholar 

  • Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657

    Google Scholar 

  • Sueoka N (1992) Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol 34:95–114

    Google Scholar 

  • Tron T, Crimi M, Colson A-M, Degli Esposti M (1991) Structure/function relationships in mitochondrial cytochrome b revealed by the kinteic and circular dichroic properties of two yeast inhibitor-resistant mutants. Eur J Biochem 199:753–760

    Google Scholar 

  • Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196

    Google Scholar 

  • Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol Phyl Evol 1:169–178

    Google Scholar 

  • Wolstenholme DR, Clary DO (1985) Sequence evolution of Drosophila mitochondrial DNA. Genetics 109:725–744

    Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nuclear substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    CAS  PubMed  Google Scholar 

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  1. Department of Genetics and Human Variation, La Trobe University, Bundoora, 3083, Victoria, Australia

    Lars S. Jermiin & Ross H. Crozier

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  1. Lars S. Jermiin
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  2. Ross H. Crozier
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Correspondence to: L.S. Jermiin

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Jermiin, L.S., Crozier, R.H. The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: Sequence divergence in hymenoptera may be associated with nucleotide content. J Mol Evol 38, 282–294 (1994). https://doi.org/10.1007/BF00176090

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  • DOI: https://doi.org/10.1007/BF00176090

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