Vol. 18 No. 2 (2023)

Molecular genetic characteristics of Darevskia portschinskii lizard populations based on microsatellite markers analysis

Irena A. Martirosyan
Institute of Gene Biology, Russian Academy of Sciences, Moscow
Dmitrii O. Odegov
Institute of Gene Biology, Russian Academy of Sciences, Moscow
Ilaha E. Kafarova
Institute of Gene Biology, Russian Academy of Sciences, Moscow
Marine S. Arakelyan
Yerevan State University, Yerevan
Alexey P. Ryskov
Institute of Gene Biology, Russian Academy of Sciences, Moscow
Vitaly I. Korchagin
Institute of Gene Biology, Russian Academy of Sciences, Moscow

Published 2023-12-27


  • Darevskia lizards,
  • Darevskia portschinskii,
  • taxonomy and population genetics,
  • microsatellite loci,
  • genetic polymorphism,
  • genetic differentiation
  • ...More

How to Cite

Martirosyan, I. A., Odegov, D. O., Kafarova, I. E., Arakelyan, M. S., Ryskov, A. P., & Korchagin, V. I. (2023). Molecular genetic characteristics of Darevskia portschinskii lizard populations based on microsatellite markers analysis. Acta Herpetologica, 18(2), 147–158. https://doi.org/10.36253/a_h-14756

Funding data


The Caucasian rock lizard species Darevskia portschinskii is one of the bisexual species participating in interspecific hybridisation as the paternal ancestor with the maternal ancestors D. mixta and D. raddei resulting in the successful formation of the parthenogenetic D. dahli and D. rostombekowi, respectively. Populations of D. portschinskii have been previously divided into two subspecies, D. p. portschinskii and D. p. nigrita according to their geographical distribution and the morphological data, but they have not been characterised genetically. Here, we used ten microsatellite markers to determine the genetic structure of the D. portschinskii populations. The utility of the developed microsatellite markers for investigating the genetic variability within and among populations with a heterogeneous spatial distribution was demonstrated. Our results showed that the intra- and interspecific differentiation of the studied populations were consistent with the morphological data on the subspecies status of the D. p. portschinskii and D. p. nigrita populations. A potential applicability of the developed microsatellite markers to study genetic diversity of Darevskia species and subspecies complexes is suggested.


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  1. Arribas, O.J. (1999): Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Merttens, 1921, Sensu Lato) and their relationships among the Eurasian Lacertid lizards. Rus. J. Herpetol. 6: 1 – 22.
  2. Badaeva, T.N., Malysheva, D.N., Korchagin, V.I., Ryskov, A.P. (2008): Genetic variation and de novo mutations in the parthenogenetic Caucasian rock lizard Darevskia unisexualis. PLoS One. 3: e2730.
  3. Bakradze, M.A. (1976): New subspecies, Lacerta portschinskii nigrita ssp. n., from Eastern Transcaucasia. Vestnik Zoologii. 4: 54 – 57. (Russian)
  4. Borkin, L.Ya., Darevskiy, I.S. (1980): Reticular (hydrogenous) speciation in vertebrates. Zh Obshch Biol. 41: 485 – 506. (Russian)
  5. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L. (2009): BLAST+: architecture and applications. BMC Bioinformatics. 10: 421.
  6. Chirhart, S.E., Honeycutt, R.L., Greenbaum, I.F. (2005): Microsatellite variation and evolution in the Peromyscus maniculatus species group. Mol. Phylogenet. Evol. 34: 408 – 415.
  7. Darevsky, I. S. (1967): Rock lizards of the Caucasus (systematics, ecology, and phylogeny of the polymorphic group of Caucasian lizards of the subgenus Archaeolacerta). Leningrad. otd., L.: Nauka.
  8. Dobzhansky, Th. (1937): Genetics and the Origin of Species. New York.: Columbia Univ. Press.
  9. Earl, D.A. and vonHoldt, B.M. (2012): STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359 - 361
  10. Ellegren, H. (2004): Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5: 435 − 445.
  11. Estoup, A. and Cornuet, J.-M. (1999): Microsatellite evolution: inferences from population data. In: Microsatellites: Evolution and Applications, p. 49 – 65. Goldstein, D.B. and Schlötterer, C., Eds., Oxford University Press, New York
  12. Estoup, A., Garnery, L., Solignac, M., Cornuet, J.-M. (1995): Microsatellite variation in honey bee (Apis mellifera L.) populations: Hierarchical genetic structure and test of the infinite allele and stepwise mutation model. Genetics. 140: 679 – 695.
  13. Evanno, G., Regnaut, S., Goudet, J. (2005): Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14: 2611 – 2620.
  14. Goudet, J. (2005): Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes. 5: 184 – 186.
  15. Harr, B., Weiss, S., David, J.R., Brem, G., Schlötterer, C. (1998): A microsatellite-based multilocus phylogeny of the Drosophila melanogaster species complex. Curr. Biol. 8: 1183 – 1187.
  16. Hedrick, P.W. (2005): A Standardized Genetic Differentiation Measure. Evolution. 59: 1633 – 1638.
  17. Hughes, M., Möller, M., Bellstedt, D.U., Edwards, T.J., De Villiers, M. (2005): Refugia, dispersal and divergence in a forest archipelago: a study of Streptocarpus in eastern South Africa. Mol. Ecol. 14: 4415 – 4426.
  18. Jarne, P., Lagoda, P.J. (1996): Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11: 424 – 429.
  19. Jombart, T. (2008): adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 24: 1403 – 1405.
  20. Jombart, T., Ahmed, I. (2011): adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. 27: 3070 – 3071.
  21. Jombart, T., Devillard, S. and Balloux, F. (2010): Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics. 11.
  22. Kamvar, Z.N., Tabima, J.F., Grünwald, N.J. (2014): Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281.
  23. Kankare, M., Van Nouhuys, S., Hanski, I. (2005): Genetic divergence among host-specific cryptic species in Cotesia melitaearum Aggregate (Hymenoptera: Braconidae), parasitoids of checkerspot butterflies. Ann. Entomol. Soc. Am. 98: 382 – 394.
  24. Kessler, K. (1878): Journey through the Transcaucasian region in 1875 with a zoological purpose. In: Proceedings of the St. Petersburg Society of Naturalists, 8: Appendix. p. 160 – 163. A. Beketov, A., Ed., St. Petersburg.
  25. Knaden, M., Tinaut, A., Cerda, X., Wehner, S., Wehner, R. (2005): Phylogeny of three parapatric species of desert ants, Cataglyphis bicolor, C. viatica, and C. savignyi: A comparison of mitochondrial DNA, nuclear DNA, and morphological data. Zoology. 108: 169 – 177.
  26. Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A., Mayrose, I. (2015): Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 15: 1179 - 1191.
  27. Korablev, M.P., Korablev, N.P., Korablev, P.N. (2018): Genetic Polymorphism and Population Structure of the Introduced American Mink (Neovison Vison Schreber, 1777) in the Center of European Russia by Means of Microsatellite Loci. Rus. J. Genetics. 54: 1179 – 1184.
  28. Koressaar, T. and Remm, M. (2007): Enhancements and modifications of primer design program Primer3. Bioinformatics. 23: 1289 – 1291.
  29. MacCulloch, R.D., Murphy, R.W., Fu, J., Darevsky, I.S., Danielyan, F.D. (1997): Disjunct habitats as islands: genetic variability in the Caucasian rock lizard Lacerta portschinskii. Genetica. 101: 41 – 45.
  30. Meirmans, P.G, Hedrick, P.W. (2011): Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11: 5-18.
  31. Mikulíˇcek, P., Crnobrnja-Isailovi´c, J., Piálek, J. (2007): Can microsatellite markers resolve phylogenetic relationships between closely related crested newt species (Triturus cristatus superspecies)? Amphibia-Reptilia. 28: 467 – 474.
  32. Nei, M. (1972): Genetic Distance between Populations. The American Naturalist. 106: 283 – 292.
  33. Nei, M. (1987): Molecular Evolutionary Genetics, New York Chichester, West Sussex: Columbia University Press.
  34. Ochkalova, S., Korchagin, V., Vergun, A., Urin, A., Zilov, D., Ryakhovsky, S., Girnyk, A., Martirosyan, I., Zhernakova, D.V., Arakelyan, M., Danielyan, F., Kliver ,S., Brukhin, V., Komissarov, A., Ryskov, A. (2022): First Genome of Rock Lizard Darevskia valentini Involved in Formation of Several Parthenogenetic Species. Genes. 13: 1569.
  35. Orsini, L., Huttunen, S., Schlötterer, C. (2004): A multilocus microsatellite phylogeny of the Drosophila virilis group. Heredity. 93: 161 – 165.
  36. Paradis, E. (2010): pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics. 26: 419 – 420.
  37. Peréz, T., Albornoz, J., Domingues, A. (2002): Phylogeography of chamois (Rupicapra spp.) inferred from microsatellites. Mol. Phylogenet. Evol. 25: 524 – 534.
  38. Petren, K., Grant, B.R., Grant, P.R. (1999): A phylogeny of Darwin’s finches based on microsatellite DNA length variation. Proc. Biol. Sci. 266: 321 – 329.
  39. Petren, K., Grant, P.R., Grant, B.R., Keller, L.F. (2005): Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol. Ecol. 14: 2943-2957.
  40. Petrosyan, V., Osipov, F., Bobrov, V., Dergunova, N., Omelchenko, A., Varshavskiy, A., Danielyan, F., Arakelyan, M. (2020): Species Distribution Models and Niche Partitioning among Unisexual Darevskia dahli and Its Parental Bisexual (D. portschinskii, D. mixta) Rock Lizards in the Caucasus. Mathematics. 8: 1329.
  41. Pritchard, J.K., Stephens, M., Donnelly, P. (2000): Inference of population structure using multilocus genotype data. Genetics. 155: 945 – 959.
  42. Quinlan, A.R., Hall, I.M. (2010): BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 26: 841 – 842.
  43. R Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  44. Rato, C., Stratakis, M., Sousa-Guedes, D., Sillero, N., Corti, C., Freitas, S., D. Harris, J., Carretero, M.A. (2021): The more you search, the more you find: Cryptic diversity and admixture within the Anatolian rock lizards (Squamata, Darevskia) // Zool. Scr. 50: 193 – 209.
  45. Richard, M., Thorpe, R.S. (2001): Can microsatellites be used to infer phylogenies? Evidence from population affinities of the western Canary Island Lizard (Gallotia galloti). Mol. Phylogenet. Evol. 20: 351 – 360.
  46. Semenova, A.V., Stroganov, A.N., Bugaev, A.V., Rubtsova, G.A, Malutina, A.M. (2019): An Analysis of Microsatellite Polymorphism in the Population of the Arctic Rainbow Smelt Osmerus dentex from Eastern and Western Kamchatka. Rus. J. Genetics. 55: 79 – 88.
  47. Thiel, T., Michalek, W., Varshney, R., Graner, A. (2003): Exploiting EST databases for the development and characterisation of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106: 411 – 422
  48. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M. and Rozen, S.G. (2012): Primer3 – new capabilities and interfaces. Nucleic Acids Res. 40: 115.
  49. Uzzell, T. and Darevsky, I.S. (1975): Biochemical evidence for the hybrid origin of the parthenogenetic species of Lacerta saxicola complex (Sauria, Lacertidae) with a discussion of some ecological and evolutionary implications. Copeia. 1975: 204 – 222.