Organisms Diversity & Evolution (2018) 18:355–366 https://doi.org/10.1007/s13127-018-0375-5 ORIGINAL ARTICLE 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. Borovikova1,2 & Valentina S. Artamonova2,3 Received: 25 July 2017 /Accepted: 30 July 2018 /Published online: 4 August 2018 # Gesellschaft für Biologische Systematik 2018 Abstract 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. Keywords Vendace . Morphological characters . Allopatric origin . Phylogenetic lineages . Lake Pleshcheyevo Introduction ecological divergence and significant genetic polymorphism are usually revealed in these populations. Scenarios where two Coregonids are considered to be a good model for postglacial or more phylogenetic lineages are almost nondistinguishable evolution investigations, adaptive radiation, and ecological by morphological characters are uncommon (April et al. speciation research (Svärdson 1979; Douglas et al. 1999; 2011). However, these situations are important for studying Hudson et al. 2007; Bernatchez et al. 2010; Symonová et al. the mechanisms of formation of morphological uniformity 2013). Heterogeneous coregonid populations are useful for under conditions of genetic differentiation. studying the processes involved during secondary contact of The model for this investigation is a vendace Coregonus two or more phylogenetic lineages with allopatric origin albula (Linnaeus, 1758) population of Lake Pleshcheyevo (Bernatchez and Dodson 1990;Østbyeetal.2005;Hudson (the Upper Volga basin) with a high level of intrapopulation et al. 2011;Dellingetal.2014). Considerable morpho- genetic polymorphism (Borovikova 2017). This population is the southernmost vendace population in the primary species range in European Russia (Fig. 1). Vendace of this population * Elena A. Borovikova differ from vendace of other lakes in a larger body size; spec- [email protected] imens caught in the early twentieth century were as long as 30 cm and weighed as much as 300 g (Borisov 1924), al- 1 Laboratory of Fish Ecology, Papanin Institute for Biology of Inland though, according to our data, the mean size and weight have Waters RAS, Borok, Yaroslavl region, Russia 152742 decreased, respectively, to 18–20 cm and 50–80 g by now. 2 Institute of Biophysics Siberian Branch of RAS, Akademgorodok, Comparison with C. albula populations of other water bodies Krasnoyarsk, Russia 660036 allowed Borisov (1924) to regard Lake Pleshcheyevo vendace 3 Severtsov Institute of Ecology and Evolution RAS, Leninski prosp., as a separate form, C. albula L. natio nova pereslavicus;later, 33, Moscow, Russia 119071 356 Borovikova E.A., Artamonova V.S. Fig. 1 Map of European north of Russia marking the selected sampling location. 1, 2—Lake Goreloye [16] and Lake Bol’shoye Krasnoye [35] (Bol’shoy Solovetsky Island); 3—Lake Beloye [16]; 4—Lake Pleshcheyevo: lineages E [44] and ALBP2 [29]; 5—Lake Vishtynetskoye (Kaliningrad region) [28]. In square brackets, the sample size is shown Berg (1962) raised it to the rank of subspecies, C. albula individuals by nucleotide substitutions in 32 sites. Thirty- pereslavicus. At present, Russian ichthyologists consider one polymorphic sites were placed into encoding gene of sub- vendace of Lake Pleshcheyevo to be a local form of vendace unit 1 of the NADH dehydrogenase complex. Twenty-nine (Reshetnikov 2010); therefore, it is not included in FishBase nucleotide substitutions were synonymous, but two substitu- (www.fishbase.org/). This form is unique to the National Park tions led to point mutations in the second position of the 2nd BLake Pleshcheyevo^ andislistedintheRedDataBookof and 97nd codons. Both of these nonsynonymous substitutions the Russian Federation (2001). resulted in replacement of the amino acid isoleucine by thre- The molecular genetic polymorphism of the vendace pop- onine (Borovikova 2017). The level of genetic differentiation ulation of this water body was analyzed in the framework of between lineages measure up 1.56% (p distance, two- the long-term project BComprehensive study of the Lake parametric Kimura model (Kimura 1980)). At the same time, Pleshcheyevo ecosystem^ carried out by the Papanin the mean p distance value for vendace and peled (C. peled) Institute for Biology of Inland Waters of the Russian haplotypes is 0.23%, and for vendace and whitefish (C. Academy of Sciences. Two regions of mitochondrial DNA lavaretus), haplotype is about 2.2% (Borovikova 2017). were used as polymorphism markers: a 5′ fragment of the The results of analysis of the COI polymorphism con- cytochrome oxidase subunit I gene (coI) 585 base pairs (bp) firmed the data for the ND1 fragment. The individuals of in length (the COI fragment) and a fragment containing the different lineages were the carriers of different COI haplo- complete nucleotide sequence of subunit I of the NADH de- types. These sequence variants were distinguished by nucleo- hydrogenase complex (nd1), as well as the adjacent regions of tide substitutions at six sites, five of which were synonymous 16S rDNA and leucine tRNA at the 5′ end and isoleucine and and did not lead to changes in the amino acid sequence in the glutamine tRNAs at the 3′ end (the ND1 fragment). protein molecule. Similarly to the ND1 fragment, the level of Restriction analysis of 2052 bp and sequencing of 1906 bp COI intrapopulational polymorphism of vendace of Lake of this sequence have been performed. Pleshcheyevo was high and reached five nucleotide substitu- The results of the genetic analysis have demonstrated that tions, or 0.97%. For example, according to Schlei et al. two mitochondrial DNA (mtDNA) phylogenetic lineages of (2008), the level of intraspecific differentiation of the COI vendace (E and ALBP2) coexist in Lake Pleshcheyevo, with a for the genus Coregonus varies from 0.0 to 0.77%. At the high genetic differentiation between them. Thus, according to same time, despite the sequence divergence between lineages analysis of polymorphism of the ND1 fragment, the ALBP2 E and ALBP2, they still group with other C. albula lineages to specimens’ sequences differ from sequences of the E the exclusion of other Coregonus species (Borovikova 2017). Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula... 357 Thus, these lineages have diverged so much that they could Vendace specimens were caught from 2013 to 2015 in have been regarded as different species if they had not lived in compliance with the permissions for fishing and hunting for the same lake and had been distinguishable from each other in wildlife species included in the Red Data Book of the Russian catches on the basis of external characters. In addition, until Federation no. 51 of March 21, 2013; no. 136 of August 28, now, no groups of vendace have been identified in the lake, 2013; no. 38 of April 11, 2014; and no. 7 of February 25, differing in the place and time of spawning. 2015. For fishing, we used pelagic and bottom gillnets with The application of the 1.0–1.5% sequence divergence per a mesh size of 18–25 mm. Pelagic nets were placed at a depth million year molecular clock for salmonid mtDNA (Shed’ko of 0 to 5 m, and bottom nets were placed in water 15–17 m et al. 1996) would suggest that the ancestral forms of two depth in several stationary locations of the lake. Nets were set lineages diverged about one million years ago during the and pulled at sunrise or sunset and fished for 3–12 h. In addi- Pleistocene period. Undoubtedly, these lineages developed tion, since ALBP2 vendace were few, we included additional under allopatric conditions and have populated Lake specimens of this lineage collected in 2005 (Table 1). Pleshcheyevo independently of each other. Lineage E is cur- To fulfill the purpose of comparing morphological features rently dominant in the lake. Representatives of this lineage are of two vendace lineages, it was important to identify the rep- also most frequently found in other water bodies of Eurasia. resentatives of these lineages in the samples. Therefore, the Representatives of the phylogenetically older lineage ALBP2 following research procedure was developed. Each specimen coexisting with lineage E in Lake Pleshcheyevo currently ac- was assigned a unique number, and tissue samples for molec- count for 5–6% of the total population.