SpringerLink
Log in

Low Level of Resistance to Anticoagulant Rodenticides in the Vkorс1 Gene in House Mice (Mus musculus) and Norway Rats (Rattus norvegicus) in Russia

  • Published:
Russian Journal of Biological Invasions Aims and scope Submit manuscript

Abstract

Genetic resistance to anticoagulants caused by mutations in the Vkorc1 gene of the most invasive rodent species—Norway rats and house mice, has not been studied in Russia. We analyzed the variability of the Vkorc1 gene in house mice and Norway rats in various settlements of Russia, and identified mutations responsible for resistance to rodenticides. Two exons of the Vkorc1 gene were analyzed in 71 Norway rats from four cities (Moscow, Tyumen, Chita, Rostov-on-Don) and 108 house mice from cities and small settlements (Moscow region, Tormosin, Nizhny Tsasuchei). Three Norway rats (15.8% of the studied individuals) in Moscow have a heterozygous state the Tyr139Ser mutation, which is responsible for resistance. House mice were not found to have mutations in the Vkorc1 gene responsible for resistance to anticoagulants of the first and second generation in the Leu128Ser and Tyr139Cys positions located in the third exon. However, in cities in the first exon, we identified two heterozygous mutations have not be described previously in the scientific literature: Lys58Arg and Ser31Trp. In Russia, the genetic resistance to rodenticides in settlements in the populations of house mice and Norway rats is significantly lower than in Western Europe.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Boyle, C.M., Case of apparent resistance of Rattus norvegicus Berkenhout to anticoagulant poisons, Nature, 1960, vol. 188, no. 4749, p. 517.

  2. Buckle, A.P., Anticoagulant resistance in the United Kingdom and a new guideline for the management of resistant infestations of Norway rats (Rattus norvegicus Berk.), Pest Manage. Sci., 2013, vol. 69, no. 3, pp. 334–341.

    Article  CAS  Google Scholar 

  3. Buckle, A., Endepols, S., Klemann, N., and Jacob, J., Resistance testing and the effectiveness of difenacoum against norway rats (Rattus norvegicus) in a tyrosine139cysteine focus of anticoagulant resistance, Westphalia, Germany, Pest Manage. Sci., 2013, vol. 69, no. 2, pp. 233–239.

    Article  CAS  Google Scholar 

  4. Buckle, A., Jones, C., Talavera, M., and Prescott, C., Anticoagulant Resistance in Rats and Mice in the UK—Summary Report with New Data for 2019–2020. Report from the Campaign for Responsible Rodenticide Use (CRRU) UK for the Government Oversight Group, Vertebrate Pests Unit, Univ. of Reading, UK, 2020. http://www.thinkwildlife.org/. Accessed October 6, 2020.

  5. Capizzi, D., Bertolino, S., and Mortelliti, A., Rating the rat: Global patterns and research priorities in impacts and management of rodent pests, Mammal Rev., 2014, vol. 44, no. 2, pp. 148–162.

    Article  Google Scholar 

  6. Dodsworth, E., Mice are spreading despite such poisons as warfarin, Munic. Eng. London, 1961, vol. 3746, p. 1668.

    Google Scholar 

  7. Duncan, B.J.M.L., Koenders, A., Burnham, Q., and Lohr, M.T., Mus musculus populations in Western Australia lack VKORC1 mutations conferring resistance to first generation anticoagulant rodenticides: Implications for conservation and biosecurity, PLoS One, 2020, vol. 9, 0236234. https://doi.org/10.1371/journal.pone.0236234

  8. Endepols, S., Buckle, A., Eason, C., Pelz, H.J., Meyer, A., Berny, P., et al., RRAC Guidelines on Anticoagulant Rodenticide Resistance Management. Technical Report, Croplife International, Brussles, 2015, pp. 1–30.

  9. Espinosa, M.B., Efficacy of anticoagulant drugs as rodenticides and genetic variation on Vkorc1 of Mus musculus from Buenos Aires province (Argentina), J. Basic Appl. Genet., 2013, vol. 24, no. 1, pp. 27–31.

    Google Scholar 

  10. Goulois, J., Lambert, V., Legros, L., Benoit, E., and Lattard, V., Adaptative evolution of the Vkorc1 gene in Mus musculus domesticus is influenced by the selective pressure of anticoagulant rodenticides, Ecol. Evol., 2017, vol. 7, no. 8, pp. 2767–2776.

    Article  Google Scholar 

  11. Hall, T.A., BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT, Nucleic Acids Res., 1999, vol. 41, pp. 95–98.

    CAS  Google Scholar 

  12. Haniza, M.Z., Adams, S., Jones, E.P., Macnicoll, A., Mallon, E.B., Smith, R.H., and Lambert, M.S., Large-scale structure of brown rat (Rattus norvegicus) populations in England: Effects on rodenticide resistance, Peer J., 2015, vol. 3, p. 1458.

    Article  Google Scholar 

  13. Iannucci, A., Natali, C., Capizzi, D., Sinibaldi, I., Sposimo, P., Ciofi, C., and Fratini, S., First record of VKORC1 sequence mutation associated with resistance to anticoagulant rodenticides in Italian individuals of Mus musculus domesticus, Hystrix, Ital. J. Mammol., 2019, vol. 30, pp. 183–185.

  14. Jones, C., Talavera, M., Buckle, A., and Prescott, C., Anticoagulant Resistance in Rats and Mice in the UK—Summary Report with New Data for 2019. Report from the Campaign for Responsible Rodenticide Use (CRRU) UK for the Government Oversight Group, Vertebrate Pests Unit, University of Reading, UK, 2019. www.thinkwildlife.org/downloads_resources/. Accessed September, 18, 2020.

  15. Korobitsina, K.B. and Yakimenko, L.V., The role and place of wagneri-like forms of house mouse (Rodentia, Muridae) in the fauna of Russia and adjacent countries, Zool. Zh., 2004, vol. 83, pp. 1081–1030.

    Google Scholar 

  16. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., Mega X: Molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, pp. 1547–1549.

    Article  CAS  Google Scholar 

  17. Li, T., Chang, C.Y., **, D.Y., Lin, P.J., Khvorova, A., and Stafford, D.W., Identification of the gene for vitamin K epoxide reductase, Nature, 2004, vol. 427, pp. 541–544.

    Article  CAS  Google Scholar 

  18. Ma, X., Wang, D., Li, N., Liu, L., Tian L., Luo, C., et al., Low warfarin resistance frequency in Norway rats in two cities in China after 30 years of usage of anticoagulant rodenticides, Pest Manage. Sci., 2018, vol. 74, no. 11, pp. 2555–2560.

    Article  CAS  Google Scholar 

  19. Maltsev, A.N., Stakheev, V.V., Bogdanov, A.S., Fomina, E.S., and Kotenkova, E.V., Phylogenetic relationships of intraspecific forms of the house mouse Mus musculus: Analysis of variability of the control region (D-loop) of mitochondrial DNA, Dokl. Biol. Sci., 2015, vol. 465, no. 3, pp. 285–288.

    Article  CAS  Google Scholar 

  20. Maltsev, A.N., Stakheev, V.V., and Kotenkova, E.V., Role of invasions in formation of phylogeographic structure of house mouse (Mus musculus) in some areas of Russia and the near abroad, Russ. J. Biol. Invasions, 2016, vol. 7, no. 2, pp. 255–267.

    Article  Google Scholar 

  21. McGee, C.F., McGilloway, D.A., and Buckle, A.P., Anticoagulant rodenticides and resistance development in rodent pest species: A comprehensive review, J. Stored Prod. Res., 2020, vol. 88, 101688.

  22. Meerburg, B.G., Van Gent-Pelzer, M.P., Schoelitsz, B., Esther, A., and Van der Lee, T.A., Distribution of anticoagulant rodenticide resistance in Rattus norvegicus in the Netherlands according to Vkorc1 mutations, Pest Manage. Sci., 2014, vol. 70, no. 11, pp. 1761–1766.

    Article  CAS  Google Scholar 

  23. Mironova, T.A., Rylnikov, V.A., Bogacheva, A.V., and Lavrenchenko, L.A., Distribution of vkorc1 gene mutations and resistance of gray rats to anticoagulant rodenticides in a number of Russian cities, Pest-Menedzhment, 2020, vol. 1, pp. 5–7.

    Google Scholar 

  24. Mooney, J., Lynch, M.R., Prescott, C.V., Clegg, T., Loughlin, M., Hannon, B., et al., VKORC1 sequence variants associated with resistance to anticoagulant rodenticides in Irish populations of Rattus norvegicus and Mus musculus domesticus, Sci. Rep., 2018, vol. 8, 4535.https://doi.org/10.1038/s41598-018-22815-7

  25. OEPP/EPPO EPPO Standard PP 2/1(1). Guideline on good plant protection practice: Principles of good plant protection practice, OEPP/EPPO Bull., 1994, vol. 24, pp. 233–240.

  26. Oldenburg, J., Marinova, M., Müller-Reible, C., and Watzka, M., The vitamin K cycle, Vitam. Horm., 2008, vol. 78, pp. 35–62.

    Article  CAS  Google Scholar 

  27. Pelz, H.J., Rost, S., Hunerberg, M., Fregin, A., Heiberg, A.C., Baert, K., et al., The genetic basis of resistance to anticoagulants in rodents, Genetics, 2005, vol. 170, no. 4, pp. 1839–1847.

    Article  CAS  Google Scholar 

  28. Pelz, H.J., Rost, S., Müller, E., Esther, A., Ulrich, R.G., and Müller, C.R., Distribution and frequency of Vkorc1 sequence variants conferring resistance to anticoagulants in Mus musculus, Pest Manage. Sci., 2012, vol. 68, pp. 254–259.

    Article  CAS  Google Scholar 

  29. Petrosyan, V.G. and Khlyap, L.A., Samye opasnye invazionnye vidy Rossii (TOP-100) (The Most Dangerous Invasive Species in Russia (TOP-100)), Dgebuadze, Yu.Yu., Petrosyan, V.G., and Khlyap, L.A., Eds., Moscow: KMK, 2018.

  30. Pocock, M.J., Searle, J.B., and White, P.C., Adaptations of animals to commensal habitats: Population dynamics of house mice Mus musculus domesticus on farms, J. Anim. Ecol., 2004, vol. 73, no. 5, pp. 878–888.

    Article  Google Scholar 

  31. Prager, E.M., Tichy, H., and Sage, R.D., Mitochondrial DNA sequence variation in the eastern house mouse, Mus musculus: Comparison with other house mice and report of a 75-bp tandem repeat, Genetics, 1996, vol. 143, pp. 427–446.

    Article  CAS  Google Scholar 

  32. Prescott, C., Resistance to the anticoagulant rodenticides— the deployment of the new molecular methodology to identify mutations of the VKORC1 resistance gene, and understanding their potential impact on treatment outcome, Pest Menedzhment, 2013, vol. 88, no. 4, pp. 39–46.

    Google Scholar 

  33. Prescott, C.V., Buckle, A.P., Gibbings, J.G., Allan, EdN.W., and Stuart, A.M., Anticoagulant resistance in Norway rats (Rattus norvegicus Berk.) in Kent—A VKORC1 single nucleotide polymorphism, tyrosine139phenylalanine, new to the UK, Int. J. Pest Manage., 2010, vol. 57, no. 1, pp. 61–65.

    Article  Google Scholar 

  34. Rost, S., Fregin, A., Ivaskevicius, V., Conzelmann, E., Hörtnagel, K., Pelz, H.J., Lappegard, K., Seifried, E., Scharrer, I., Tuddenham, E.G., Müller, C.R., Strom, T.M., and Oldenburg, J., Mutations in VKORC1 cause warfarin resistance and multiple coagulation factor deficiency type 2, Nature, 2004, vol. 427, no. 6974, pp. 537–541.

    Article  CAS  Google Scholar 

  35. Rost, S., Pelz, H.J., Menzel, S., Conzelmann, E., Macnicoll, A.D., León, V., Song, K.J., Jäkel, T., Oldenburg, J., and Müller C.R., Novel mutations in the VKORC1 gene of wild rats and mice-a response to 50 years of selection pressure by warfarin?, BMC Genet., 2009, vol. 10, no. 1, pp. 1–9.

    Article  Google Scholar 

  36. Spiridonova, L.N., Introgression of nuclear and mitochondrial DNA markers of Mus musculus musculus to aboriginal populations of wild mice from Central Asia (M. m. wagneri) and South Siberia (M. m. gansuensis), Mol. Biol., 2014, vol. 48, pp. 75–83.

    Article  CAS  Google Scholar 

  37. Unified register of certificates of state registration in the Russian Federation, 2020. https://portal.eaeunion.org.

Download references

Funding

This research was supported by the Russian Science Foundation, project no. 19-74-00148.

Author information

Authors and Affiliations

  1. Severtsov Institute of Problems of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    A. N. Maltsev & E. V. Kotenkova

  2. The Federal Research Center Southern Scientific Centre of the Russian Academy of Sciences, 344006, Rostov-on-Don, Russia

    V. V. Stakheev

  3. Scientific Research Institute for Systems Biology and Medicine, Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing, 117246, Moscow, Russia

    A. N. Maltsev, S. V. Ryabov & T. V. Gololobova

  4. Tyumen State University, 625003, Tyumen, Russia

    S. N. Gashev

  5. Institute of Natural Resources, Ecology and Cryology, Siberian Branch, Russian Academy of Sciences, 672014, Chita, Russia

    Yu. A. Bazhenov

Authors
  1. A. N. Maltsev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. V. Stakheev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Ryabov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. V. Gololobova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. N. Gashev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu. A. Bazhenov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. V. Kotenkova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to A. N. Maltsev, V. V. Stakheev, S. V. Ryabov, T. V. Gololobova, S. N. Gashev, Yu. A. Bazhenov or E. V. Kotenkova.

Ethics declarations

Conflict of interest. The author declares that she has no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maltsev, A.N., Stakheev, V.V., Ryabov, S.V. et al. Low Level of Resistance to Anticoagulant Rodenticides in the Vkorс1 Gene in House Mice (Mus musculus) and Norway Rats (Rattus norvegicus) in Russia. Russ J Biol Invasions 13, 392–397 (2022). https://doi.org/10.1134/S2075111722030109

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2075111722030109

Keywords:

Search

Navigation