Journal of Molecular Evolution

, Volume 64, Issue 3, pp 308–320 | Cite as

Unusual Origin of a Nuclear Pseudogene in the Italian Wall Lizard: Intergenomic and Interspecific Transfer of a Large Section of the Mitochondrial Genome in the Genus Podarcis (Lacertidae)

  • Martina Podnar
  • Elisabeth Haring
  • Wilhelm Pinsker
  • Werner Mayer


Two distinct cytochrome b-like sequences were discovered in the genome of Podarcis sicula. One of them represents a nuclear copy of a mitochondrial sequence (numt-sic) differing by 14.3% from the authentic mitochondrial (mt) sequence obtained from the same individual. This numt, however, differs by only 2.7% from the mt sequence found in one population of Podarcis muralis, a related species in which no corresponding numt was detected. The numt-sic sequence extends over at least 7637 bp and is homologous to a section of the mt genome spanning from the tRNA-Lys to the tRNA-Pro gene. Premature mt stop codons were detected in two of the nine protein coding genes of numt-sic. The distribution of substitutions among the three codon positions and the transition/transversion ratio of the numt-sic sequence resemble, with few exceptions, those of functional mt genes, indicating a rather recent transfer to the nucleus. Phylogenetic analyses performed on the data set including P. sicula numt-cytb sequences as well as mt-cytb sequences from the same individuals and mt sequences of various P. muralis populations suggest that numt-sic originated in P. muralis. In a geographic survey, P. sicula populations belonging to different mt lineages, covering most of the distribution area, were screened for the presence of numt-sic and for a 15-bp duplication polymorphism in the numt-nd5 sequence. Our results suggest that numt-sic has spread rapidly through the species range via sexual transmission, thereby being transferred to populations belonging to well-separated mt lineages that diverged 1–3 Mya.


numt Mitochondrial DNA Lacertidae Podarcis sicula P. muralis Interspecific transfer 



The authors want to express their thanks to R. Godinho (Porto), Đ. Ugarković (Zagreb), and P. Wihlidal (Vienna) for valuable technical advice. We are also obliged to L. Kruckenhauser, F. Nittinger, and M. Pavlicev for valuable comments on the manuscript. The study was partially supported by the Research Fund of the Republic of Croatia, project no. 183007.

Supplementary material

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Supplementary material


  1. Arctander P (1995) Comparison of a mitochondrial gene and a corresponding nuclear pseudogene. Proc R Soc Lond B 262:13–19CrossRefGoogle Scholar
  2. Beckman KB, Smith MF, Orrego C (1993) Purification of mitochondrial DNA with WizardTM Minipreps DNA Purification System. Promega Notes Mag 43:10Google Scholar
  3. Bensasson D, Zhang D, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321PubMedCrossRefGoogle Scholar
  4. Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201PubMedCrossRefGoogle Scholar
  5. Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101:17747–17752PubMedCrossRefGoogle Scholar
  6. Capula M (1993) Natural hybridization in Podarcis sicula and P. wagleriana (Reptilia: Lacertidae). Biochem Syst Ecol 21:373–380CrossRefGoogle Scholar
  7. Capula M (2002) Genetic evidence of natural hybridization between Podarcis sicula and Podarcis tiliguerta (Reptilia: Lacertidae). Amphibia-Reptilia 23:313–321CrossRefGoogle Scholar
  8. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  9. Collura RV, Stewart CB (1995) Insertions and duplications of mtDNA in the nuclear genomes of Old World monkeys and hominoids. Nature 378:485–492PubMedCrossRefGoogle Scholar
  10. Densmore LD, Wright JW, Brown WM (1985) Length variation and heteroplasmy are frequent in mitochondrial DNA from parthenogenetic and bisexual lizards (genus Cnemidophorus). Genetics 110:689–707PubMedGoogle Scholar
  11. Fu J (2000) Toward the phylogeny of the family Lacertidae—why 4708 base pairs of mtDNA sequences cannot draw the picture. Biol J Lin Soc 71:203–217CrossRefGoogle Scholar
  12. Goldman N, Anderson JP, Rodrigo AG (2000) Likelihood-based tests of topologies in phylogenetics. Syst Biol 49:652–670PubMedCrossRefGoogle Scholar
  13. Gorman GC, Soulé M, Yang SY, Nevo E (1975) Evolutionary genetics of insular Adriatic lizards. Evolution 29:52–71CrossRefGoogle Scholar
  14. Gruschwitz M, Böhme W (1986) Podarcis muralis (Laurenti, 1768)—Mauereidechse. In: Böhme W (ed) Handbuch der Amphibien und Reptilien Europas, Echsen III (Podarcis). Aula-Verlag, Wiesbaden, pp 155–208Google Scholar
  15. Hall T (2004) BioEdit Sequence Alignment Editor, version 6.0.7. Isis Pharmaceuticals, Carlsbad, CAGoogle Scholar
  16. Harris DJ, Arnold EN (1999) Relationships of wall lizards, Podarcis (Reptilia: Lacertidae) based on mitochondrial DNA sequences. Copeia 1999:749–754CrossRefGoogle Scholar
  17. Harris DJ, Pinho C, Carretero MA, Corti C, Böhme W (2005) Determination of genetic diversity within insular lizard Podarcis tiliguerta using mtDNA sequence data, with a reassessment of the phylogeny of Podarcis. Amphibia-Reptilia 26:401–407CrossRefGoogle Scholar
  18. Henle K, Klaver CJJ (1986) Podarcis sicula (Rafinesque-Schmaltz, 1810)—Ruineneidechse. In: Böhme W (ed) Handbuch der Amphibien und Reptilien Europas, Echsen III (Podarcis). Aula-Verlag, Wiesbaden, pp 254–342Google Scholar
  19. Jones CS, Tegelström H, Latchman DS, Berry RJ (1988) An improved rapid method for mitochondrial DNA isolation suitable for use in the study of closely related populations. Biochem Genet 26:83–88PubMedCrossRefGoogle Scholar
  20. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200PubMedCrossRefGoogle Scholar
  21. Kordiš D, Gubenšek F (1998) Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. Proc Natl Acad Sci USA 95:10704–10709PubMedCrossRefGoogle Scholar
  22. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245PubMedCrossRefGoogle Scholar
  23. López JV, Yuhki N, Masuda R, Modi W, O’Brien SJ (1994) Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. J Mol Evol 39:174–190PubMedGoogle Scholar
  24. Lü XM, Fu YX, Zhang YP (2002) Evolution of mitochondrial cytochrome b pseudogene in genus Nycticebus. Mol Biol Evol 19:2337–2241PubMedGoogle Scholar
  25. Moritz C, Brown WM (1986) Tandem duplication of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science 233:1425–1427PubMedCrossRefGoogle Scholar
  26. Moritz C, Brown WM (1987) Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 84:7183–7187PubMedCrossRefGoogle Scholar
  27. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  28. Passoni JC, Benozzati ML, Rodrigues MT (2000) Mitochondrial DNA polymorphism and heteroplasmy in populations of the three species of Tropidurus of the nanuzae group (Squamata, Tropiduridae). Gen Mol Biol 23:351–356Google Scholar
  29. Pinho C, Ferrand N, Harris DJ (2006) Reexamination of the Iberian and North African Podarcis (Squamata: Lacertidae) phylogeny based on increased mitochondrial DNA sequencing. Mol Phylogenet Evol 38:266–273PubMedCrossRefGoogle Scholar
  30. Podnar M, Mayer W, Tvrtković N (2004) Mitochondrial phylogeography of the Dalmatian wall lizard, Podarcis melisellensis (Lacertidae). Org Divers Evol 4:307–317CrossRefGoogle Scholar
  31. Podnar M, Mayer W, Tvrtković N (2005) Phylogeography of the Italian wall lizard, Podarcis sicula, as revealed by mitochondrial DNA sequences. Mol Ecol 14:575–588PubMedCrossRefGoogle Scholar
  32. Posada D, Crandall KA (1998) ModelTest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  33. Poulakakis N, Lymberakis P, Antoniou A, Chalkia D, Zouros E, Mylonas M,Valakos E (2003) Molecular phylogeny and biogeography of the wall-lizard Podarcis erhardii (Squamata: Lacertidae). Mol Phylogenet Evol 28:38–46PubMedCrossRefGoogle Scholar
  34. Richly E, Leister D (2004) NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 21:1081–1084PubMedCrossRefGoogle Scholar
  35. Rodriguez FJ, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501PubMedGoogle Scholar
  36. Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  37. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  38. Smith MF, Thomas WK, Patton JL (1992) Mitochondrial DNA-like sequence in the nuclear genome of an akodontine rodent. Mol Biol Evol 9:204–215PubMedGoogle Scholar
  39. Stanton DJ, Daehler LL, Moritz CC, Brown WM (1994) Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics 137:233–241PubMedGoogle Scholar
  40. Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524PubMedGoogle Scholar
  41. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MAGoogle Scholar
  42. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees Mol Biol Evol 10:512–526PubMedGoogle Scholar
  43. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  44. Wellehan JFX, Johnson AJ (2005) Reptile virology. Vet Clin Exot Anim 8:27–52CrossRefGoogle Scholar
  45. Williams ST, Knowlton N (2001) Mitochondrial pseudogenes are pervasive and often insidous in the snapping shrimp genus Alpheus. Mol Biol Evol 18:1484–1493PubMedGoogle Scholar
  46. Zhang DX, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251CrossRefGoogle Scholar
  47. Zischler H, Geisert H, von Haeseler A, Pääbo S (1995) A nuclear ‘fossil’ of the mitochondrial D-loop and the origin of modern humans. Nature 378:489–492PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Martina Podnar
    • 1
    • 2
  • Elisabeth Haring
    • 1
  • Wilhelm Pinsker
    • 1
  • Werner Mayer
    • 1
  1. 1.Molecular Systematics, 1st Zoological DepartmentMuseum of Natural History ViennaViennaAustria
  2. 2.Department of ZoologyCroatian Natural History MuseumZagrebCroatia

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