Organisms Diversity & Evolution

, Volume 18, Issue 3, pp 355–366 | Cite as

Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula) population in Lake Pleshcheyevo (the Volga River basin): relationships of two phylogenetic lineages in a new zone of secondary contact

  • Elena A. BorovikovaEmail author
  • Valentina S. Artamonova
Original Article


This is the report about the secondary contact zone of coregonids in the Upper Volga basin. Two mitochondrial DNA (mtDNA) phylogenetic lineages of vendace Coregonus albula (Linnaeus, 1758) living in Lake Pleshcheyevo have been analyzed and compared in terms of morphological characters. These lineages have developed under the conditions of allopatry and are characterized by strong differences of the mitochondrial DNA sequences. The lineages have coexisted in the same lake since the last glaciation maximum (about 10,000 years ago). The morphological analysis has shown that representatives of both lineages correspond to C. albula, while slight, morphological variations between lineages indicate different food preferences and locomotor abilities. Scenarios where multiple distinct coexisting phylogenetic lineages are characterized by low levels of morpho-ecological divergence are uncommon. These situations are important for understanding biodiversity dynamics and the mechanisms that drive coexistence, adaptive divergence, hybridization, and extinction when genetically divergent lineages meet in secondary contact.


Vendace Morphological characters Allopatric origin Phylogenetic lineages Lake Pleshcheyevo 



We are grateful to M.Yu. Fedorov, director of the National Park “Lake Pleshcheyevo,” as well as the personnel of the national park and our colleagues from IBIW RAS, for various help in collecting the material; Yulia V. Kodukhova and Nina V. Raushkina for the assistance in measurements; Alexei A. Bolotovski, Dmitri P. Karabanov, Alexander A. Makhrov, Mikhail I. Malin, and Alexei K. Smirnov for valuable comments and discussion of the manuscript.

Funding information

The preparation of this manuscript was supported by the Russian Science Foundation, grant no. 16-14-10001.

Compliance with ethical standards

This article does not contain any studies with human participants performed by any of the authors. Vendace were caught in compliance with the permission for fishing and hunting for wildlife objects included in the Red Data Book of the Russian Federation no. 51 of March 21, 2013; no. 136 of August 28, 2013; no. 38 of April 11, 2014; and no. 7 of February 25, 2015.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aleyev, Y. G. (1957). Characteristics and topography of fish fins’ functions [Harakteristika i topografiya funkcij plavnikov ryby]. Voprosy ihtiologii, 8, 55–76.Google Scholar
  2. April, J., Mayden, R. L., Hanner, R. H., & Bernatchez, L. (2011). Genetic calibration of species diversity among North America’s freshwater fishes. Proceedings of the National Academy of Sciences of the USA, 108(26), 10602–10607. Scholar
  3. Berg, L. S. (1962). Freshwater fishes of the U.S.S.R. and adjacent countries, 1. Jerusalem: Israel Program for Scientific Translations.Google Scholar
  4. Bernatchez, L., & Dodson, J. J. (1990). Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis. Evolution, 44(5), 1263–1271. Scholar
  5. Bernatchez, L., Renaut, S., Whiteley, A. R., Derome, N., Jeukens, J., Landry, L., Lu, G., Nolte, A. W., Østbye, K., Rogers, S. M., & St-Cyr, J. (2010). On the origin of species: insights from the ecological genomics of lake whitefish. Philosophical Transactions of the Royal Society B, 365, 1783–1800. Scholar
  6. Bochkarev, N. A., Zuykova, E. I., Abramov, S. A., Katokhin, A. V., Matveev, A. A., Samusenok, V. P., Baldina, S. N., Gordon, N. Y., & Politov, D. V. (2013). Morphological, ecological and mtDNA sequence variation in coregonid fish from the Baunt Lake system (the Vitim River basin). Advanced Limnology, 64, 257–277. Scholar
  7. Borisov, P. G. (1924). Vendace of Lake Pereslavskoye [Ryapushka ozera Pereslavskogo]. Trudy NIRKh, 1, 53–127.Google Scholar
  8. Borovikova, E. A. (2017). Special traits of the genetic structure and origin of the population of vendace Coregonus albula of Pleshcheyevo Lake. Biology Bulletin, 44(3), 245–250. Scholar
  9. Borovikova, E. A., Alekseeva, Y. I., Schreider, M. J., Artamonova, V. S., & Makhrov, A. A. (2013). Morphology and genetics of the ciscoes (Actinopterygii: Salmoniformes: Salmonidae: Coregoninae: Coregonus) from the Solovetsky Archipelago (White Sea) as a key to determination of the taxonomic position of ciscoes in Northeastern Europe. Acta Ichthyologica et Piscatoria, 43(3), 183–194. Scholar
  10. Chugunova, N. I. (1952). Methods for age and growth study [Metodika izucheniya vozrasta i rosta ryb]. Moscow: Sovetskajya nauka.Google Scholar
  11. Darroch, J. N., & Mosimann, J. E. (1985). Canonical and principal components of shape. Biometrika, 72, 241–252. Scholar
  12. Delling, B., Palm, S., Palkopoulou, E., & Prestegaard, T. (2014). Genetic signs of multiple colonization events in Baltic ciscoes with radiation into sympatric spring and autumn spawners confined to early postglacial arrival. Ecology and Evolution, 4(22), 4346–4360. Scholar
  13. Douglas, M. R., Brunner, P. C., & Bernatchez, L. (1999). Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine region of Europe represent species flocks? Molecular Ecology, 8, 589–603. Scholar
  14. Dyatlov, M. A. (1978). About populational heterogeneity of the vendace Coregonus albula L. of Lake Ladoga [O populyatsionnoy neodnorodnosti ryapushki Coregonus albula L. Ladozhskogo ozera]. Voprosy ikhtiologii, 18(4), 615–623.Google Scholar
  15. Ecosystem of Lake Pleshcheyevo [Ekosistema ozera Pleshcheyevo]. (1989). Leningrad: Nauka.Google Scholar
  16. Hudson, A. G., Vonlanthen, P., Mueller, R., & Seehausen, O. (2007). Review: the geography of speciation and adaptive radiation in coregonines. In M. Jankun, P. Brzuzan, P. Hliawa, & M. Luczynski (Eds.), Biology and management of coregonid fishes – 2005, 60 (pp. 111–146). Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung.Google Scholar
  17. Hudson, A. G., Vonlanthen, P., & Seehausen, O. (2011). Rapid parallel adaptive radiations from a single hybridogenic ancestral population. Philosophical Transactions of the Royal Society B, 278, 58–66. Scholar
  18. Huxley, J. S. (1924). Constant differential growth – ratios and their significance. Nature, 114, 895–896. Scholar
  19. Huxley, J. S. (1932). Problems of relative growth. New York: Dial Press.Google Scholar
  20. Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. Scholar
  21. Lazzaro, X. (1987). A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia, 146(2), 97–167. Scholar
  22. Linnaeus, C. (1758). Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, 1. Editio decima, reformata. Holmia, Stockholm: Laurentii Salvii.Google Scholar
  23. Lleonart, J., Salat, J., & Torres, G. J. (2000). Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. Scholar
  24. Lombarte, A., & Lleonart, J. (1993). Otolith size changes related with body growth, habitat depth and temperature. Environmental Biology of Fishes, 37, 297–306. Scholar
  25. Malin, M. I., Zhdanova, S. M., Bazarov, M. I., Borisenko, E. S., Malina, Y. I. & Tsvetkov, A. I. (2014). Vertical distribution and migration of vendace (Coregonus albula L.) in Lake Pleshcheyevo. Abstracts 12th International symposium on the biology and management of coregonid fishes 25–30 August, 2014. (p. 48). Irkutsk: Asprint.Google Scholar
  26. Mehner, T., Pohlmann, K., Elkin, C., Monaghan, M. T., Nitz, B., & Freyhof, J. (2010). Genetic population structure of sympatric and allopatric populations of Baltic ciscoes (Coregonus albula complex, Teleostei, Coregonidae). BMC Evolutionary Biology, 10, 85–98. Scholar
  27. Ohlberger, J., Mehner, T., Staaks, G., & Hölker, F. (2008a). Temperature-related physiological adaptations promote ecological divergence in a sympatric species pair of temperate freshwater fish, Coregonus spp. Functional Ecology, 22, 501–508. Scholar
  28. Ohlberger, J., Staaks, G., Petzoldt, T., Mehner, T., & Hölker, F. (2008b). Physiological specialization by thermal adaptation drives ecological divergence in a sympatric fish species pair. Evolutionary Ecology Research, 10, 1173–1185.Google Scholar
  29. Oreha, J., & Skute, N. (2009). Morphological characteristics of local populations of European vendace Coregonus albula (L.) in some lakes of Latvia during 50 years. Proceedings of the Latvian Academy of Sciences. Section B, 63(6), 271–278. Scholar
  30. Østbye, K., Bernatchez, L., Næsje, T. F., Himberg, K.-J. M., & Hindar, K. (2005). Evolutionary history of the European whitefish Coregonus lavaretus (L.) species complex as inferred from mtDNA phylogeography and gill-raker numbers. Molecular Ecology, 14, 4371–4387. Scholar
  31. Pakkasmaa, S., & Piironen, J. (2000). Water velocity shapes juvenile salmonids. Evolutionary Ecology, 14(8), 721–730. Scholar
  32. Perelygin, A. A (1988). Genetic variability of proteins in the populations of vendace (Coregonus albula) and least cisco (Coregonus sardinella) [Populyatsionno-geneticheskiy analiz belkov evropeyskoy (Coregonus albula) i sibirskoy (Coregonus sardinella) ryapushek]. PhD Thesis. Novosibirsk: Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences.Google Scholar
  33. Pokrovskii, V. V. (1967). About morphological features, origin and geographical distribution Coregonus sardinella maris-albi Berg [O morfologicheskikh osobennostyakh, proiskhozhdenii i geograficheskom rasprostranenii belomorskoy ryapushki Coregonus sardinella maris-albi Berg]. Izvestiya GosNIORKh, 62, 100–114.Google Scholar
  34. Pravdin, I. F. (1966). A manual on fish studies [Rukovodstvo po izucheniyu ryb]. Moscow: Pishchevaya Promyshlennost.Google Scholar
  35. Reshetnikov, Y. S. (Ed.). (2010). Fishes of reserves of Russia. Freshwater fishes [Ryby v zapovednikah Rossii. Presnovodnye ryby]. Moscow: Publishing House KMK.Google Scholar
  36. Sandlund, O. T. (1992). Differences in the ecology of two vendace populations separated in 1895. Nordic Journal of Freshwater Research, 67, 52–60.Google Scholar
  37. Schlei, O. L., Crête-Lafrenière, A., Whiteley, A. R., Brown, R. J., Olsen, J. B., Bernatchez, L., & Wenburg, J. K. (2008). DNA barcoding of eight North American coregonine species. Molecular Ecology Resources, 8, 1212–1218. Scholar
  38. Schulz, M., Freyhof, J., Saint-Laurent, R., Østbye, K., Mehner, T. & Bernatchez, L. (2006). Evidence for independent origin of two spring-spawning ciscoes (Salmoniformes: Coregonidae) in Germany. Journal of Fish Biology, 68(Suppl. A), 119–135, doi:
  39. Shed’ko, S. V., Ginatulina, L. K., Parpura, I. Z., & Ermolenko, A. V. (1996). Evolutionary and taxonomic relationships among Far-Eastern salmonid fishes inferred from mitochondrial DNA divergence. Journal of Fish Biology, 49, 815–829. Scholar
  40. Smitt, F. A. (1886). Kritisk förteckning öfver de i Riksmuseum befintliga salmonider. Kongl. Sv. Vet. Akademiens Handlingar. Stockholm: P. A. Norstedt & Söner.Google Scholar
  41. Sokal, R. R., & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research (3rd ed.). New York: Freeman.Google Scholar
  42. StatSoft, Inc. STATISTICA (data analysis software system), version 10. 2011. Google Scholar
  43. Stolbunova, V. N. (2006). Zooplankton of Lake Pleshcheyevo [Zooplankton ozera Pleshcheyevo]. Moscow: Nauka.Google Scholar
  44. Svärdson, G. (1979). Speciation of Scandinavian Coregonus. Report of the Institute of Freshwater Research, Drottningholm, 57, 3–95.Google Scholar
  45. Symonová, R., Majtánová, Z., Sember, A., Staaks, G. B. O., Bohlen, J., Freyhof, J., Rábová, M., & Ráb, P. (2013). Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evolutionary Biology, 13(1), 42. Scholar
  46. The Red Data Book of the Russian Federation (Animals) (2001). Moscow: Astrel’.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2018

Authors and Affiliations

  1. 1.Laboratory of Fish EcologyPapanin Institute for Biology of Inland Waters RASYaroslavl regionRussia
  2. 2.Institute of Biophysics Siberian Branch of RASKrasnoyarskRussia
  3. 3.Severtsov Institute of Ecology and Evolution RASMoscowRussia

Personalised recommendations