Eur. J. Entomol. 119: 99-110, 2022 | DOI: 10.14411/eje.2022.011

Mitochondrial DNA variation of Drosophila obscura (Diptera: Drosophilidae) across EuropeOriginal article

Pavle ERIĆ ORCID...1, 5, Marina STAMENKOVIĆ-RADAK ORCID...2, 5, Milan DRAGIĆEVIĆ ORCID...1, Maaria KANKARE ORCID...3, 5, Megan A. WALLACE ORCID...4, 5, Marija SAVIĆ VESELINOVIĆ ORCID...2, 5, Mihailo JELIĆ ORCID...2, 5
1 Institute for Biological Research "Siniša Stanković", National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11000 Belgrade, Serbia; e-mails: pavle.eric@ibiss.bg.ac.rs, mdragicevic@ibiss.bg.ac.rs
2 University of Belgrade, Faculty of Biology, Studentski trg 16, 11000 Belgrade, Serbia; e-mails: marina@bio.bg.ac.rs, marijas@bio.bg.ac.rs, mihailoj@bio.bg.ac.rs
3 Department of Biological and Environmental Science, University of Jyväskylä, Survontie 9, 40014 Jyväskylä, Finland; e-mail: maaria.kankare@jyu.fi
4 Institute of Evolutionary Biology, University of Edinburgh, Charlotte Auerbach Road, Kings Buildings, Edinburgh EH9 3FL, UK; current e-mail: M.A.Wallace@exeter.ac.uk
5 The European Drosophila Population Genomics Consortium (DrosEU)

Drosophila obscura is a common fruit fly that inhabits the temperate forests of Europe. While it is abundant in the north compared to other Drosophila, its density decreases southwards, where it is gradually replaced by other Drosophila species. This study describes variation in the mitochondrial Cyt b gene of D. obscura from several European populations. We observed a large number of haplotypes, together with the structuring of genetic variation. Genetic variation is higher in the west where O1 and related divergent haplotypes dominate. In the east, the O2 haplotype is most frequent, together with haplotypes that recently arose from it. In the central part of the species range, both O1 and O2 are equally present, along with many others. These data reveal signs of population expansions that probably happened earlier in the west, and more recently in the east. Though our conclusions are based on only one genetic marker, limiting the power of the analysis, the results imply either postglacial expansion from two unique sources or, more likely, eastwards stepping-stone expansion. This study adds important information on genetic variation and phylogeography to the obscure biology of D. obscura, a species that has the potential to become an interesting model in evolutionary biology and conservation genetics.

Keywords: Cyt b, genetic variation, population expansion, phylogeography

Received: April 12, 2021; Revised: December 20, 2021; Accepted: December 20, 2021; Published online: February 9, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
ERIĆ, P., STAMENKOVIĆ-RADAK, M., DRAGIĆEVIĆ, M., KANKARE, M., WALLACE, M.A., SAVIĆ VESELINOVIĆ, M., & JELIĆ, M. (2022). Mitochondrial DNA variation of Drosophila obscura (Diptera: Drosophilidae) across Europe. EJE119, Article 99-110. https://doi.org/10.14411/eje.2022.011
Download citation

References

  1. Akaike H. 1973: Information theory and an extension of the maximum likelihood principle. In Petrov B.N. & Csaki F. (eds): Proceedings of the 2nd International Symposium on Information Theory, Tsahkadsor, Armenia, USSR, September 2-8, 1971. Akademiai Kiado, Budapest, pp. 267-281.
  2. Anderson W., Dobzhansky T., Pavlovsky O., Powell J. & Yardley D. 1975: Genetics of natural populations XLII. Three de­cades of genetic change in Drosophila pseudoobscura. - Evolution 29: 24-36. Go to original source...
  3. Bachmann L. & Sperlich D. 1993: Gradual evolution of a specific satellite DNA family in Drosophila ambigua, D. tristis, and D. obscura. - Mol. Biol. Evol. 10: 647-659.
  4. Balanyá J., Oller J.M., Huey R.B., Gilchrist G.W. & Serra L. 2006: Global genetic change tracks global climate warming in Drosophila subobscura. - Science 313: 1773-1775. Go to original source...
  5. Ballard J.W. & Kreitman M. 1994: Unraveling selection in the mitochondrial genome of Drosophila. - Genetics 138: 757-772. Go to original source...
  6. Bandelt H.J., Forster P. & Rohl A. 1999: Median-joining networks for inferring intraspecific phylogenies. - Mol. Biol. Evol. 16: 37-48. Go to original source...
  7. Begon M. 1978: Population densities in Drosophila obscura Fallén and D. subobscura Collin. - Ecol. Entomol. 3: 1-12. Go to original source...
  8. Beribaka M., Dimkić I., Jelić M., Stanković S., Pržulj N., Anđelković M. & Stamenković-Radak M. 2021: Altered diversity of bacterial communities in two Drosophila species under laboratory conditions and lead exposure. - Arch. Biol. Sci. 73: 17-29. Go to original source...
  9. Bouckaert R., Vaughan T.G., Barido-Sottani J., Duchene S., Fourment M., Gavryushkina A., Heled J., Jones G., Kühnert D., De Maio N. et al. 2019: BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. - PLoS Comput. Biol. 15(4): e1006650, 28 pp. Go to original source...
  10. Brehm A. & Krimbas C.B. 1991: Inversion polymorphism in Drosophila obscura. - J. Hered. 82: 110-117. Go to original source...
  11. Brito P.H. & Edwards S.V. 2009: Multilocus phylogeography and phylogenetics using sequence-based markers. - Genetica 135: 439-455. Go to original source...
  12. Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J. & Holmes S.P. 2016: DADA2: High-resolution sample inference from Illumina amplicon data. - Nat. Methods 13: 581-583. Go to original source...
  13. Castro J.A., Barrio E., González A., Picornell A., Ramon M.M. & Moya A. 2010: Nucleotide diversity of a ND5 fragment confirms that population expansion is the most suitable explanation for the mtDNA haplotype polymorphism of Dro­so­phila subobscura. - Genetica 138: 819-829. Go to original source...
  14. Christie J.S., Picornell A., Moya A., Ramon M.M. & Castro J.A. 2010: Dynamics of the mtDNA haplotype variability in a Drosophila subobscura population over a two-year period. - Open Evol. J. 4: 23-30. Go to original source...
  15. Erić P., Jelić M., Savić-Veselinović M., Kenig B., Anđelković M. & Stamenković-Radak M. 2019: Nucleotide diversity of Cyt b gene in Drosophila subobscura Collin. - Genetika 51: 213-226. Go to original source...
  16. Excoffier L. & Lischer H.E.L. 2010: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. - Mol. Ecol. Resour. 10: 564-567. Go to original source...
  17. Eyre-Walker A. 2002: Changing effective population size and the McDonald-Kreitman test. - Genetics 162: 2017-2024. Go to original source...
  18. Fay J.C. & Wu C.I. 2000: Hitchhiking under positive Darwinian selection. - Genetics 155: 1405-1413. Go to original source...
  19. Fragata I., Balanya J., Rego C., Matos M., Rezende E.L. & Santos M. 2010: Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura. - J. Evol. Biol. 23: 112-123. Go to original source...
  20. Fu Y.X. 1997: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. - Genetics 147: 915-925. Go to original source...
  21. Fu Y.X. & Li W.H. 1993: Statistical tests of neutrality of mutations. - Genetics 133: 693-709. Go to original source...
  22. Gao J.J., Watabe H.A., Aotsuka T., Pang J.F. & Zhang Y.P. 2007: Molecular phylogeny of the Drosophila obscura species group, with emphasis on the Old World species. - BMC Evol. Biol. 7: 87, 12 pp. Go to original source...
  23. García-Martínez J., Castro J.A., Ramón M., Latorre A. & Moya A. 1998: Mitochondrial DNA haplotype frequencies in natural and experimental populations of Drosophila subobscura. - Genetics 149: 1377-1382. Go to original source...
  24. Grant W.S. 2015: Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. - J. Hered. 106: 333-346. Go to original source...
  25. Haag-Liautard C., Coffey N., Houle D., Lynch M., Charlesworth B. & Keightley P.D. 2008: Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. - PLoS Biol. 6(8): e204, 9 pp. Go to original source...
  26. Hall T. 2011: BioEdit: an important software for molecular biology. - GERF Bull. Biosci. 2: 60-61.
  27. Heled J. & Drummond A.J. 2008: Bayesian inference of population size history from multiple loci. - BMC Evol. Biol. 8: 289, 15 pp. Go to original source...
  28. Hewitt G.M. 2004: Genetic consequences of climatic oscillations in the Quaternary. - Philos. Trans. R. Soc. Lond. (B) 359: 183-195. Go to original source...
  29. Hurst G.D. & Jiggins F.M. 2005: Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. - Proc. Biol. Sci. 272: 1525-1534. Go to original source...
  30. Jelić M., Arnqvist G., Novičić Z.K., Kenig B., Tanasković M., Anđelković M. & Stamenković-Radak M. 2015: Sex-specific effects of sympatric mitonuclear variation on fitness in Droso­phila subobscura. - BMC Evol. Biol. 15: 135, 9 pp. Go to original source...
  31. Kaneko M., Satta Y., Matsuura E.T. & Chigusa S.I. 1993: Evolution of the mitochondrial ATPase 6 gene in Drosophila: unusually high level of polymorphism in D. melanogaster. - Genet. Res. 61: 195-204. Go to original source...
  32. Kapun M., Barrón M.G., Staubach F., Obbard D.J., Wiberg R.A.W., Vieira J., Goubert C., Rota-Stabelli O., Kankare M., Bogaerts-Márquez M. et al. 2020: Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses. - Mol. Biol. Evol. 37: 2661-2678. Go to original source...
  33. Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M. & Glockner F.O. 2013: Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-gene­ration sequencing-based diversity studies. - Nucleic Acids Res. 41(1): e1, 11 pp. Go to original source...
  34. Krimbas C.B. 1993: Drosophila subobscura: Biology, Genetics, and Inversion Polymorphism. Dr. Kovac, Hamburg, 395 pp.
  35. Kurbalija Novičić Z., Sayadi A., Jelić M. & Arnqvist G. 2020: Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA. - BMC Evol. Biol. 20(1): 20, 9 pp. Go to original source...
  36. Lakovaara S. & Saura A. 1971: Genetic variation in natural populations of Drosophila obscura. - Genetics 69: 377-384. Go to original source...
  37. Librado P. & Rozas J. 2009: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. - Bioinformatics 25: 1451-1452. Go to original source...
  38. Mantel N. 1967: The detection of disease clustering and a generalized regression approach. - Cancer Res. 27: 209-220.
  39. Martinez D., Moya A., Latorre A. & Fereres A. 1992: Mitochondrial DNA variation in Rhopalosiphum padi (Homoptera: Aphididae) populations from four Spanish localities. - Ann. Entomol. Soc. Am. 85: 241-246. Go to original source...
  40. McDonald J.H. & Kreitman M. 1991: Adaptive protein evolution at the Adh locus in Drosophila. - Nature 351: 652-654. Go to original source...
  41. Meiklejohn C.D., Montooth K.L. & Rand D.M. 2007: Positive and negative selection on the mitochondrial genome. - Trends Genet. 23: 259-263. Go to original source...
  42. Nachman M.W. 1998: Deleterious mutations in animal mitochondrial DNA. - Genetica 102-103: 61-69. Go to original source...
  43. Nachman M.W., Boyer S.N. & Aquadro C.F. 1994: Nonneutral evolution at the mitochondrial NADH dehydrogenase subunit 3 gene in mice. - Proc. Natl. Acad. Sci. USA 91: 6364-6368. Go to original source...
  44. Nachman M.W., Brown W.M., Stoneking M. & Aquadro C.F. 1996: Nonneutral mitochondrial DNA variation in humans and chimpanzees. - Genetics 142: 953-963. Go to original source...
  45. Ohta T. 1992a: The nearly neutral theory of molecular evolution. - Annu. Rev. Ecol. Syst. 23: 263-286. Go to original source...
  46. Ohta T. 1992b: Theoretical study of near neutrality. II. Effect of subdivided population structure with local extinction and recolonization. - Genetics 130: 917-923. Go to original source...
  47. O'Neill S.L., Giordano R., Colbert A.M., Karr T.L. & Robertson H.M. 1992: 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. - Proc. Natl. Acad. Sci. USA 89: 2699-2702. Go to original source...
  48. Paradis E. 2010: pegas: an R package for population genetics with an integrated-modular approach. - Bioinformatics 26: 419-420. Go to original source...
  49. Pascual M., Aquadro C.F., Soto V. & Serra L. 2001: Microsatellite variation in colonizing and palearctic populations of Drosophila subobscura. - Mol. Biol. Evol. 18: 731-740. Go to original source...
  50. Pavković-Lučić S., Savić T., Jelić M., Kenig B., Tanasković M., Stamenković-Radak M. & Anđelković M. 2012: Note on the fauna of Drosophila (Diptera: Drosophilidae) and the first record of Opomyza florum (Diptera: Opomyzidae) from Mt. Goč, Serbia. - Acta Entomol. Serb. 17: 45-51.
  51. Posada D. 2008: jModelTest: phylogenetic model averaging. - Mol. Biol. Evol. 25: 1253-1256. Go to original source...
  52. Powell J.R. 1997: Progress and Prospects in Evolutionary Biology: The Drosophila Model. Oxford University Press, New York, 776 pp. Go to original source...
  53. R Development Core Team 2018: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. URL: https://www.R-project.org/
  54. Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018: Posterior summarization in bayesian phylogenetics using Tracer 1.7 - Syst. Biol. 67: 901-904. Go to original source...
  55. Ramos-Onsins S.E. & Rozas J. 2002: Statistical properties of new neutrality tests against population growth. - Mol. Biol. Evol. 19: 2092-2100. Go to original source...
  56. Rand D.M. & Kann L.M. 1996: Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. - Mol. Biol. Evol. 13: 735-748. Go to original source...
  57. Rand D.M. & Kann L.M. 1998: Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. - Genetica 102: 393-407. Go to original source...
  58. Rand D.M., Dorfsman M. & Kann L.M. 1994: Neutral and non-neutral evolution of Drosophila mitochondrial DNA. - Genetics 138: 741-756. Go to original source...
  59. Rogers A.R. & Harpending H. 1992: Population growth makes waves in the distribution of pairwise genetic differences. - Mol. Biol. Evol. 9: 552-569.
  60. Savić Veselinović M., Kurbalija Novičić Z., Kenig B., Jelić M., Patenković A., Tanasković M., Pertoldi C., Stamenković-Radak M. & Anđelković M. 2019: Local adaptation at fine spatial scale through chromosomal inversions and mito-nuclear epistasis: Findings in Drosophila subobscura (Diptera: Drosophilidae). - Eur. J. Entomol. 116: 492-503. Go to original source...
  61. Schaeffer S.W., Goetting-Minesky M.P., Kovacevic M., Peoples J.R., Graybill J.L., Miller J.M., Kim K., Nelson J.G. & Anderson W.W. 2003: Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. - Proc. Natl. Acad. Sci. USA 100: 8319-8324. Go to original source...
  62. Shorrocks B. 1975: The distribution and abundance of woodland species of British Drosophila (Diptera: Drosophilidae). - J. Anim. Ecol. 44: 851-864. Go to original source...
  63. Stamenković-Radak M., Milanović M., Savić T. & Anđelković M. 2003: Adaptive significance of amylase polymorphism in Drosophila XIII. Old World obscura species subgroup divergence according to biochemical properties of α-amylase. - Genes Genet. Syst. 78: 23-28. Go to original source...
  64. Stanić S., Kekić V. & Pavković-Lučić S. 2002: A contribution to knowledge of Drosophilidae (Diptera) fauna in Kragujevac basin. - Acta Entomol. Serb 1: 151-154.
  65. Tajima F. 1989: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. - Genetics 123: 585-595. Go to original source...
  66. Templeton A.R. 1996: Contingency tests of neutrality using intra/interspecific gene trees: The rejection of neutrality for the evolution of the mitochondrial cytochrome oxidase II gene in the hominoid primates. - Genetics 144: 1263-1270. Go to original source...
  67. Thompson J.D., Higgins D.G. & Gibson T.J. 1994: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. - Nucleic Acids Res. 22: 4673-4680. Go to original source...
  68. Wang Q., Garrity G.M., Tiedje J.M. & Cole J.R. 2007: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. - Appl. Environ. Microbiol. 73: 5261-5267. Go to original source...
  69. Weinreich D.M. & Rand D.M. 2000: Contrasting patterns of nonneutral evolution in proteins encoded in nuclear and mitochondrial genomes. - Genetics 156: 385-399. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.