Eur. J. Entomol. 118: 344-354, 2021 | DOI: 10.14411/eje.2021.036

Genetic implications of a biological invasion: Chromosomal and DNA barcode monomorphism in Old World populations of Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)Original article

Gayane KARAGYAN ORCID...1, Vladimir LUKHTANOV ORCID...2, Meri MAZMANYAN1, Ilona STEPANYAN1, Tigran GHREJYAN ORCID...1, Alena ABAKUMOVA3, Oxana NESTEROVA ORCID...3
1 Scientific Center of Zoology and Hydroecology, NAS RA, P. Sevak 7, Yerevan 0014, Armenia; e-mails: gaykaragyan@yahoo.com, meriliv33@gmail.com, ilonastepanyan37@gmail.com, tkredjyan@gmail.com
2 Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia; e-mail: lukhtanov@mail.ru
3 Belarusian State University, Faculty of Biology, Kurchatova 10, Minsk 220045, Belarus; e-mails: helen.a.2013@mail.ru, oxanesterova@gmail.com

Once introduced into new area, invasive species can be expected to have low genetic diversity due to the founder effect. Here we tested this prediction using cytogenetic and molecular analysis of Armenian and Belarusian populations of Colorado potato beetle Leptinotarsa decemlineata (Say, 1824) and by comparing the results with those of native (North America) and those introduced into Europe. This revealed that the karyotype of males from Armenia and Belarus is remarkably conserved with 2n = 35 (34 + X0), n = 17AA + X0; and includes a pair of large acrocentric chromosomes. Thus, these populations belong to the so-called acrocentric chromosome race of the Colorado potato beetle. At diakinesis there are clearly visible argentophilic signals, probably NORs (the nucleolus organizer regions) present on some autosomal bivalents, while the X chromosome was homogenously argentophilic during different stages of meiosis. C-banding revealed a small amount of constitutive heterochromatin weakly visible in the pericentromeric regions of some chromosomes. Analysis of the DNA-barcode fragment of the gene cytochrome c oxidase subunit I (COI) revealed a single haplotype (we call it "the European haplotype") and lack of inter-population variability in all the samples collected from different locations in Armenia and Belarus. The comparison of our karyological and molecular data with that available in the literature and GenBank shows that all the populations studied from the Old World are monomorphic with respect to karyotype and the mitochondrial DNA-barcode. We assume that (1) the presence of acrocentric chromosomes in the karyotype and (2) the European haplotype of mitochondrial genome are the ancestral states for all populations in the Old World and inherited from the New World invaders who colonized Europe 100 years ago. New World populations are polymorphic with respect to karyotype and mitochondrial genes; however, the European haplotype has not yet been found in America. We believe that in the future it will be found in North America, which will shed light on the origin of populations of this dangerous pest in Eurasia.

Keywords: Coleoptera, Chrysomelidae, Leptinotarsa decemlineata, Colorado potato beetle, invasion, Old World, chromosome, COI, DNA barcoding, taxonomy

Received: April 14, 2021; Revised: October 12, 2021; Accepted: October 12, 2021; Published online: November 12, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
KARAGYAN, G., LUKHTANOV, V., MAZMANYAN, M., STEPANYAN, I., GHREJYAN, T., ABAKUMOVA, A., & NESTEROVA, O. (2021). Genetic implications of a biological invasion: Chromosomal and DNA barcode monomorphism in Old World populations of Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). EJE, 118, Article 344-354. https://doi.org/10.14411/eje.2021.036
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Alyokhin A. 2009: Colorado potato beetle management on potatoes: current challenges and future prospects. - Fruit Veg. Cereal Sci. Biotech. 3 (Special Issue 1): 10-19.
    2. Azeredo-Espin A.M.L., Schroder R.F.W., Huettel M.D. & Sheppard W.S. 1991: Mitochondrial DNA variation in geographic populations of Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrisomelidae). - Experientia 47: 483-485. Go to original source...
    3. Azeredo-Espin A.M.L., Schroder R.F.W., Roderick G.K. & Sheppard W.S. 1996: Intraspecific mitochondrial DNA variation in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Biochem. Genet. 34: 253-268. Go to original source...
    4. Barton N.H. & Charlesworth B. 1984: Genetic revolutions, founder effects, and speciation. - Annu. Rev. Ecol. Syst. 15: 133-164. Go to original source...
    5. Baus Lonèar M., Paiæ F. & Ugarkoviæ Ð. 2005: Molecular cytogenetic study of heterochromatin in some coleopteran insects. - Entomol. Croat. 9(1-2): 47-56.
    6. Boiteau G. 1994: Genetics of the Colorado potato beetles, Leptinotarsa decemlineata (Say). In Jolivet P.H., Cox M.L. & Petitpierre (eds): Novel Aspects of the Biology of Chrysomelidae. Kluwer, Dordrecht, pp. 231-236. Go to original source...
    7. Brechko E.V., Elisovetskaya D.S., Nastas T.N., Voitka D.V. & Yankouskaya A.N. 2016: Formation of phenotypic structure of Colorado potato beetle (Leptinotarsa decemlineata Say) populations under ecological stress conditions. - Proc. Nat. Acad. Sci. Belarus (Agrar. Ser.) 4: 79-89 [in Russian].
    8. Capinera J.L. 2001: Handbook of Vegetable Pests. Academic Press, San Diego, 729 pp.
    9. Cohen Z.P., Brevik K., Chen Y.H., Hawthorne D.J., Weibel B.D. & Schoville S.D. 2021: Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say). - Mol. Ecol. 30: 237-254. Go to original source...
    10. Conger A.D. & Fairchild L.M. 1953: A quick-freeze method for making smear slides permanent. - Stain Technol. 28: 289-293. Go to original source...
    11. Crossley M.S., Chen Y.C., Groves R.L. & Schoville S.D. 2017: Landscape genomics of Colorado potato beetle provides evidence of polygenic adaptation to insecticides. - Mol. Ecol. 26: 6284-6300. Go to original source...
    12. De Wilde J. & Hsiao T.H. 1981: Geographic diversity of the Colorado potato beetle and its infestation in Eurasia. In Lashomb J.H. & Casagrande R.A. (eds): Advances in Potato Pest Management. Hutchinson Ross, Stroudsburg, PA, pp. 47-68.
    13. Dlugosch K.M. & Parker I.M. 2008: Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. - Mol. Ecol. 17: 431-449. Go to original source...
    14. Fasulati S.R. 1993: Polymorphism, environmental groups, and microevolution of Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera, Chrysomelidae). In: Species and Its Productivity in the Range. Gidrometeoizdat, St. Petersburg, pp. 260-262 [in Russian].
    15. Felsenstein J. 1985: Confidence limits on phylogenies: an approach using the bootstrap. - Evolution 39: 783-791. Go to original source...
    16. Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. 1994: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. - Mol. Mar. Biol. Biotechnol. 3: 294-299.
    17. Grapputo A. 2006: Development and characterization of microsatellite markers in the Colorado potato beetle, Leptinotarsa decemlineata. - Mol. Ecol. Notes 6: 1177-1179. Go to original source...
    18. Grapputo A., Boman S., Lindström L., Lyytinen A. & Mappes J. 2005: The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. - Mol. Ecol. 14: 4207-4219. Go to original source...
    19. Greenstone M.H., Rowley D.L., Weber D.C., Payton M.E. & Hawthorne D.J. 2007: Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. - Bull. Entomol. Res. 97: 201-209. Go to original source...
    20. Guénin H.A. & Scherler M. 1951: La formule chromosomiale du doryphore Leptinotarsa decemlineata Stal. - Rev. Suisse Zool. 58: 359-370.
    21. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Window 95/98/NT. - Nucl. Acids Symp. Ser. 41: 95-98.
    22. Hawthorne D.J. 2001: AFLP-Based genetic linkage map of the Colorado potato beetle Leptinotarsa decemlineata: sex chromosomes and a pyrethroid-resistance candidate gene. - Genetics 158: 695-700. Go to original source...
    23. Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003: Biological identifications through DNA barcodes. - Proc. R. Soc. Lond. (B) 270: 313-321. Go to original source...
    24. Hendrich L., Morinière J., Haszprunar G., Hebert P.D.N., Hausmann A., Köhler F. & Balke M. 2015: A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. - Mol. Ecol. Resour. 15: 795-818. Go to original source...
    25. Holm A.K., Elameen A., Oliver B.W., Brandsæter L.O., Fløistad I.S. & Brurberg M.B. 2018: Low genetic variation of invasive Fallopia spp. in their northernmost European distribution range. - Ecol. Evol. 8: 755-764. Go to original source...
    26. Howell W.M. & Black D.A. 1980: Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-srep method. - Experientia 36: 1014-1015. Go to original source...
    27. Hsiao T.H. 1985: Ecophysiological and genetic aspects of geographic variations of the Colorado potato beetles. In Ferro D.N. & Voss R.H. (eds): Proceedings of the Symposium on the Colorado Potato Beetle. XVIIth International Congress of Entomology. Mass. Agr. Exp. Stat. Res. Bull. 704, University of Massachusetts, Amherst, pp. 63-77.
    28. Hsiao C. & Hsiao T.H. 1982: Inheritance of three autosomal mutations in the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Can. J. Genet. Cytol. 24: 681-686. Go to original source...
    29. Hsiao T.H. & Hsiao C. 1983: Chromosomal analysis of Leptinotarsa decemlineata and Labidomera species (Coleoptera: Chrysomelidae). - Genetica 60: 139-150. Go to original source...
    30. Izzo V.M., Chen Y.H., Schoville S.D., Wang C. & Hawthorne D.J. 2018: Origin of pest lineages of the Colorado potato beetle (Coleoptera: Chrysomelidae). - J. Econ. Entomol. 111: 868-878. Go to original source...
    31. Jacobson J.W. & Hsiao Т.Н. 1983: Isozyme variation between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Ann. Entomol. Soc. Am. 76: 162-166. Go to original source...
    32. Jacques R.L. 1988: The Potato Beetles: The Genus Leptinotarsa in North America (Coleoptera, Chrysomelidae). Flora and Fauna Handbook, Vol. 3. Brill, New York, 144 pp. Go to original source...
    33. Jolivet P. 1991: Le doryphore menace l'Asie Leptinotarsa decemlineata Say 1824 (Coleoptera: Chrysomelidae). - Entomologiste 47: 29-48.
    34. Karagyan G., Lachowska D. & Kalashian M. 2012: Karyotype analysis of four jewel-beetle species (Coleoptera, Buprestidae) detected by standard staining, C-banding, AgNOR-banding and CMA3/DAPI staining. - Comp. Cytogen. 6: 183-197. Go to original source...
    35. Kress W.J., García-Robledo C., Uriarte M. & Erickson D.L. 2015: DNA barcodes for ecology, evolution, and conservation. - Trends Ecol. Evol. 30: 25-35. Go to original source...
    36. Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018: MEGA X: Molecular evolutionary genetics analysis across computing platforms. - Mol. Biol. Evol. 35: 1547-1549. Go to original source...
    37. Liu N., Li Y. & Zhang R. 2012: Invasion of Colorado potato beetle, Leptinotarsa decemlineata, in China: dispersal, occurrence, and economic impact. - Entomol. Exp. Appl. 143: 207-217. Go to original source...
    38. Lorite P., Torres M.I. & Palomeque T. 2013: Characterization of two unrelated satellite DNA families in the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera, Chrysomelidae). - Bull. Entomol. Res. 103: 538-546. Go to original source...
    39. Markovets A.F. 1950: Colorado Potato Beetle - Most Dangerous Pest of Crops of Potato. Academy of Sciences of Belorussian SSR, Minsk, 15 pp. [in Russian].
    40. Nalbandyan A.V. 1984: Regularities of the Population Dynamics of the Colorado Potato Beetle and Rational Methods of Fighting it in the Northeastern Zone of the Armenian SSR. PhD thesis, Armenian Scientific-Research Institute of Plant Protection, Yerevan, 139 pp. [in Russian].
    41. Nie R.-E., Breeschoten T., Timmermans M.J.T.N., Nadein K., Xue H.-J., Bai M., Huang Y., Yang X.-K. & Vogler A.P. 2018: The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes. - Cladistics 34: 113-130. Go to original source...
    42. Petitpierre E. 2011: Cytogenetics, cytotaxonomy and chromosomal evolution of Chrysomelinae revisited (Coleoptera, Chrysomelidae). - ZooKeys 157: 67-79. Go to original source...
    43. Petitpierre E., Segarra C., Yadav J.S. & Virkki N. 1988: Chromosome numbers and meioformulae of Chrysomelidae. In Jolivet P., Petitpierre E. & Hsiao T.H. (eds): Biology of Chrysomelidae. Kluwer, Dordrecht, pp. 161-186. Go to original source...
    44. Przybylska A., Budziszewska M., Klejdysz T., Nawrot J. & Obrêpalska-Stêplowska A. 2014: High stability of a mitochondrial genetic marker mtCOII in Polish Colorado potato beetle populations. - Am. J. Potato Res. 91: 720-725. Go to original source...
    45. Roman J. & Darling J.A. 2007: Paradox lost: genetic diversity and the success of aquatic invasions. - Trends Ecol. Evol. 22: 454-464. Go to original source...
    46. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. - Syst. Biol. 61: 539-542. Go to original source...
    47. Ro¿ek M. 2000: The C-banding technique for Coleoptera (Insecta). - Folia Biol. (Kraków) 48: 29-31.
    48. Ro¿ek M., Lachowska D., Petitpierre E. & Holecová M. 2004: C-bands on chromosomes of 32 beetle species (Coleoptera: Elateridae, Cantharidae, Oedemeridae, Cerambycidae, Chrysomelidae and Curculionidae). - Hereditas 140: 1-10. Go to original source...
    49. Rulik B., Eberle J., von der Mark L., Thormann J., Jung M., Köhler F., Apfel W., Weigel A., Kopetz A., Köhler J., et al. 2017: Using taxonomic consistency with semi-automated data pre-processing for high quality DNA barcodes. - Methods Ecol. Evol. 8: 1878-1887. Go to original source...
    50. Sidorenko A.P. & Berezovska O.P. 2002: Genetic structure of populations of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Russ. J. Genet. 38: 1256-1261. Go to original source...
    51. Sidorenko A.P., Berezovskaya O.P. & Sozinov A.A. 2000: The assessment of genetic polymorphism in populations of Colorado potato beetle Leptinotarsa decemlineata (Say) using RAPD markers. - Russ. J. Genet. 36: 526-532.
    52. Smith S.G. 1953: Chromosome numbers of Coleoptera. - Heredity 7: 31-48. Go to original source...
    53. Stevens N.M. 1906: Studies in Spermatogenesis, Part II. Carnegie Institution of Washington, Washington D.C, pp. 33-74.
    54. Udalov M.B. & Benkovskaya G.V. 2010: Polymorphism coxI gene of Colorado potato beetle in South Ural populations. - Resistant Pest Manag. Newslett. 19(2): 29-32.
    55. Udalov M.B. & Benkovskaya G.V. 2011: Population genetics of the Colorado potato beetle: From genotype to phenotype. - Russ. J. Genet. Appl. Res. 1: 321-333. Go to original source...
    56. Ushatinskaya R.S. (ed.). 1981: Colorado Potato Beetle, Leptinotarsa decemlineata Say. Phylogeny, Morphology, Physiology, Ecology, Adaptation, Natural Enemies. Nauka, Moscow, 377 pp. [in Russian].
    57. Virkki N. 1964: On the cytology of some Neotropical Chrysomelids. - Ann. Acad. Sci. Fenn. (A4, Biol.) 75: 1-25.
    58. Wieman H.L. 1910: A study of the germ cells of Leptinotarsa signaticollis. - J. Morphol. 21: 135-216. Go to original source...
    59. Yang F., Guo J., Liu N. & Zhang R. 2020: Genetic structure of the invasive Colorado potato beetle Leptinotarsa decemlineata populations in China. - J. Integ. Agr. 19: 350-359. Go to original source...
    60. Yocum G.D., Toutges M.J., Roehrdanz R.L. & Dihle P.J. 2011: Insertion of miniature subterminal inverted repeat-like elements in diapause-regulated genes in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Eur. J. Entomol. 108: 197-203. Go to original source...
    61. Zehnder G.W., Sandall L., Tisler A.M. & Powers T.O. 1992: Mitochondrial DNA diversity among 17 geographic populations of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). - Ann. Entomol. Soc. Am. 85: 234-240. Go to original source...
    62. Zhang J.J., Yang J., Li Y.C., Liu N. & Zhang R.Z. 2013: Genetic relationships of introduced Colorado potato beetle Leptinotarsa decemlineata populations in Xinjiang, China. - Insect Sci. 20: 643-654. 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.


    Return to the content