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. Individuals of lineage ular genetic analysis were taken under field conditions; after ALBP2 have not been found in other water bodies close to this that, each fish was frozen whole and stored until the results of lake. This lineage is therefore likely unique to Lake genetic analysis were obtained. Based on the data about the Pleshcheyevo (Borovikova 2017). ND1 fragment nucleotide sequences (Borovikova 2017), a The purpose of this study was to test if there is evidence fast identification method for individuals belonging to the that these two lineages are adaptively divergent and whether ALBP2 and E lineages was created. Three informative restric- they differ from vendace of other Russian water bodies. To tion enzymes (DpnII, MspI, and RsaI) were found; the poly- answer this question, we determined whether the two lineages morphism on the recognition sites of these enzymes allows are differentiated morphologically, how distinct is the differ- distinguishing representatives of two lineages. Lineage entiation, and what characters are typical of the representatives ALBP2 and dominant lineage E were characterized by specif- of each lineage. ic fragments’ patterns for each restriction endonuclease. This approach allowed us to study morphology of ALBP2 and E lineages separately. Materials and methods Morphological analysis was performed according to Pravdin’s(1966) modification of the protocol of measure- The study was conducted in Lake Pleshcheyevo which is lo- ments of coregonid fishes originally suggested by Smitt cated in Central Russia in the Upper Volga basin (56° 46′ N; (1886) (Fig. 2). Ten meristic and 28 morphological values 38° 46′ E) about 30 km northeast from Moscow (Fig. 1). The were measured: vt number of vertebrae; sp.br. number of gill lake supposedly has a glacial genesis and characterized by rakers on the first left gill arch; Dub number of unbranched 2 elliptical shape, surface area over 51 km , and maximum rays in dorsal fin; Db number of branched rays in dorsal fin; depth 25 m. Mean depth of the lake is 11 m. Importantly, Aub number of unbranched rays in anal fin; Ab number of thermal and oxygen stratification occurs during the summer branched rays in anal fin; Pub number of unbranched rays in (Malin et al. 2014). pectoral fin; Pb number of branched rays in pectoral fin; Vub Lake Pleshcheyevo is a meso/eutrophic water body (Stolbunova 2006). The ichthyofauna of the lake is represent- Table 1 Characteristics of vendace of Lake Pleshcheyevo estimated in ed by 13 species including vendace (C. albula). The dominant this study group of the fish community is Cyprinidae: roach (Rutilus sp.), common bleak (Alburnus alburnus), ide (Leuciscus Year of sampling Phylogenetic lineages idus), common bream (Abramis brama), white bream ALBP2 Е (Blicca bjoerkna), tench (Tinca tinca), and crucian carp (Carassius carassius). The second predominant family is 2005 3 – Percidae: perch (Perca fluviatilis)andruffe(Gymnocephalus 2013 – 25 cernua). Also, the lake is inhabited by burbot (Lota lota, 2014 10 19 Gadiformes), northern pike (Esox lucius, Esocidae), and 2015 16 – spined loach (Cobitis taenia, Cobitidae) (Ecosystem of Lake Total 29 44 Pleshcheyevo 1989). 358 Borovikova E.A., Artamonova V.S.

Fig. 2 The measurement scheme used for coregonid fish (Pravdin 1966, distance (aD); r–d, postdorsal distance (pD); a–z, anteventral distance modified after Smitt 1886): a–b, total length (L); a–c, fork length (Sm); a– (aV); a–y, anteanal distance (aA); f–d, caudal peduncle length (lCP); q– d, standard length (l); o–d, trunk length (CC); a–n, snout length (aO); n–p, s, dorsal fin base length (lD); t–u, dorsal fin depth (hD); y–y1,analfin horizontal diameter of eye (O); a–o, head length (C); p–o, postorbital base length (lA); e–j, anal fin depth (hA); v–x, pectoral fin length (lP); z– distance (pO); w–g, head depth through the eye (hC1); l–m, head depth z1, pelvic fin length (lV); v–z, pectroventral distance (PV); z–y, ventroanal (at nape) (hC2); a–a6, upper jaw (maxilla) length (lmx); k1–l1, lower jaw distance (VA); interorbital width—the area on top of the head between the (mandible) length (lmd); g–h, maximum body depth (H); a–q, antedorsal eye number of unbranched rays in pelvic fin; Vb number of un- range of variation of the characters studied in C. albula and branched rays in pelvic fin; Q body weight, g; L total body compared them with the same characters of Lake length, mm; Sm fork length, mm; l standard length, mm; CC Pleshcheyevo vendace, separately for lineages E and trunk length, mm; aD antedorsal distance, mm; pD postdorsal ALBP2. For all samples of vendace, the morphological anal- distance, mm; aA anteanal distance, mm; aV anteventral dis- ysis was carried out using the same protocol, all measurements tance, mm; PV pectroventral distance, mm; VA ventroanal dis- being performed by the same operator. tance, mm; H maximum body depth, mm; lCP caudal pedun- The primary results of the morphological analysis were cle length, mm; lD dorsal fin base length, mm; hD dorsal fin statistically treated as recommended by Sokal and Rohlf depth, mm; lA anal fin base length, mm; hA anal fin depth, (1995). The nonparametric Mann–Whitney U test was used mm; lV pelvic fin length, mm; lP pectoral fin length, mm; C to compare meristic characteristics of vendace of different head length, mm; hC1 head depth through the eye, mm; hC2 populations. The values of body weight (Q), total body length head depth (at nape), mm; aO snout length, mm; O horizontal (L), fork length (Sm), standard length (l), and trunk length diameter of eye, mm; pO postorbital distance, mm; iO inter- (CC) fitted the normal distribution; therefore, the mean values orbital width—the area on top of the head between the eye, of character for different samples were compared using mm; lmx upper jaw (maxilla) length, mm; lmd lower jaw Student’s t test. (mandible) length, mm. The variability of the 23 morphometric parameters (except All specimens for the morphological analysis consisted of weight and lengths of body) was investigated by canonical adult individuals. The age of fish was determined using scales discriminant function analysis (DFA). The technique accord- (Chugunova 1952). Scales were soaked in a 4% ammonia ing to Lombarte and Lleonart (1993), Lleonart et al. (2000), solution for a few minutes and then photographed with a dig- and Bochkarev et al. (2013) was used for removing allometric ™ b ital camera (TOUPCAM ) under a stereomicroscope effects. We employed the equation Zij = Yij [X0/Xj] i,whereYij Micromed MC-2-ZOOM (var. CR) (Opticheskiye pribory is measure of i morphometric parameter for j the individual; Xj [Optical devices], Saint Petersburg, Russia) at 10× or 20×. is the overall body size of the individual j, X0 is the reference Digital images were processed in Adobe Photoshop CS soft- body size, and bi is the allometric parameter relating the de- ware, and the annual rings were counted. pendent variable Yi with the independent variable X.Zij is the Since the genetic distance between the two mtDNA line- transformed measure Yij, if the fish overall body size was X0, ages corresponded to differences of the species level, it was considering its allometric growth. The geometric mean of all important to make sure that the sample of the lineage ALBP2 of the specimen’s values was used as the overall body size had no specific characteristics that could raise the question of measure Xj. The reference body size X0 is the arithmetic mean whether it actually belongs to the species C. albula. For this of all Xj (Darroch and Mosimann 1985; Bochkarev et al. purpose, we used our data on the morphological characteris- 2013). The parameter b in the allometric formula log Y =log tics of vendace from four populations of northern European a + b × log X is the allometric coefficient, characterized the Russia (Fig. 1). This information was used to determine the slope of the line in this linear equation (Huxley 1924, 1932). Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula... 359

After this conversion, all the values obtained were logarithm- respect to two parameters: number of gill rakers on the first left transformed. gill arch (sp.br.) and number of unbranched rays in dorsal fin

We performed DFA with two sets of samples. At first, we (Dub)(Table4). Moreover, considerable discrepancies for pa- included in analysis only representatives of different vendace rameters characterizing body size variability were revealed: lineages of Lake Pleshcheyevo. It was been done to explore total body length (L), fork length (Sm), standard length (l), morphometric discrimination among the ALBP2 and E line- trunk length (CC), body weight (Q). ages. Then we involved the representatives of other four sam- It is known the body size parameters of coregonids are very ples of vendace to estimate range of morphological differen- plastic and depend on the individual traits of each specimen tiation of C. albula of the water bodies of the European north such as age, growth, and maturation rates of males and fe- of Russia and compare with intrapopulational distinction of males (Oreha and Skute 2009). Therefore, we analyzed age the vendace of Lake Pleshcheyevo. of individuals and sex ratio in the E and ALBP2 lineages Discriminant functions were interpreted using the factor (Table 5). However, we could not make any conclusions about structure coefficient, which are correlations between the vari- variation in size at age because randomly the different age ables in the model and the discriminant functions. Scatterplot groups were predominant in E and ALBP2 samples (4+ and of scores for all specimens for the first two canonical discrim- 3+ age groups, respectively). Moreover, the age groups were inant functions were produced to visualize the extent of dif- different in number of specimens and were not useful for ferentiation between groups. Statistical analyses were per- correct comparison. formed using Statistica v. 10.0 software (StatSoft Inc. 2011). In order to form a more comprehensive view on the level of morphological differentiation of the two phylogenetic lineages, we used the canonical discriminant function analysis (DFA). Results Before DFA, all morphological characters were adjusted to min- imize the confounding effects of any body size differences be- A total morphological analysis was carried out for 73 speci- tween the analyzed groups (see BMaterial and methods^). mens from Lake Pleshcheyevo, among which 29 belonged to With two vendace lineages of Lake Pleshcheyevo, DFA the lineage ALBP2 and 44 to the lineage E. Tables 2 and 3 identified one canonical variable (Wilks’ λ = 0.05507; df = show the main 38 meristic and morphometric characters of 44; p < 0.000). Representatives of ALBP2 and E lineages two vendace lineage groups. The number of unbranched and were correctly classified with 100% accuracy. However, none branched rays in the anal and dorsal fins and the number of of the morphological traits makes a significant contribution to vertebrae for individuals assigned to the ALBP2 and E line- discrimination of two lineages (Table 6). ages were typical for the species C. albula (species description The results of DFA including the vendace of Lake according to www.fishbase.org/). Pleshcheyevo and specimens of other populations of Comparison of the values of the meristic characters shows European north of Russia are presented in Fig. 3 and significant differences between E and ALBP2 lineages with Table 7. With six vendace groups, DFA identified five

Table 2 Meristic traits of the two lineages of vendace of Lake parentheses), and the interval of variation are given; m—there are more Pleshcheyevo and C. albula of other water bodies of European north of than one mode value for this trait; B–^ no data Russia (for comparison). For each trait, the median, the mode (in

Traits Water bodies

Lake Pleshcheyevo Lake Beloye Lake Vishtynetskoye Lake Bol’shoye Krasnoye Lake Goreloye

Lineage E Lineage ALBP2 vt 56 (56) 51–57 56 (56) 53–57 55 (m) 53–57 56 (56) 53–59 – 57 (58) 56–59 sp.br.50(m)43–55 52 (53) 48–56 –– – 44 (44) 40–49

Dub 4(4)3–53(3)2–43(3)3–44(4)3–53(3)2–43(3)3–4

Db 9(9)7–11 9 (9) 7–10 10 (m) 9–11 9 (9) 8–11 8 (8) 7–10 9 (9) 9–10

Aub 4(4)3–43(3)2–44(4)3–44(4)3–43(3)3–44(4)3–4

Ab 12 (12) 10–14 12 (12) 10–15 13 (13) 12–14 12 (12) 10–15 12 (12) 10–15 12 (12) 11–14

Pub 1(1)1–11(1)1–11(1)1–11(1)1–11(1)1–11(1)1–1

Pb 14 (14) 12–15 14 (14) 12–15 13 (13) 12–15 14 (14) 12–15 14 (14) 11–16 14 (14) 13–14

Vub 2(2)1–22(2)1–22(2)1–22(2)2–22(2)2–2 –

Vb 10 (10) 9–11 10 (10) 9–11 10 (10) 9–10 10 (10) 9–10 10 (10) 9–11 10 (10) 9–10 360 Borovikova E.A., Artamonova V.S.

Table 3 Morphological characteristics measured in Morphological characteristics Lineages specimens of E and ALBP2 vendace lineages of Lake EALBP2 Pleshcheyevo N M±σ N M±σ Min–max Min–max

Total length (L) (mm) 44 208.7 ± 24.65 27 195.2 ± 16.96 160–244 170–233

Fork length (Sm) (mm) 44 192.9 ± 23.0 29 179.6 ± 15.41 146–225 157–215 Standard length (l) (mm) 44 182.8 ± 22.05 29 169.7 ± 14.08 139–217 149–204 Trunk length (CC) (mm) 44 144.4 ± 17.0 29 134.0 ± 11.88 108–170 117.0–161.5 Body weight (Q) (g) 44 66.8 ± 18.03 29 51.2 ± 12.74 29.2–89.0 37.0–84.1 Antedorsal distance (aD) (mm) 44 86.9 ± 11.5 29 80.9 ± 7.55 66.0–104.0 72.0–101.0 Postdorsal distance (pD) (mm) 44 80.4 ± 8.54 29 75.2 ± 6.94 60.5–93.0 63.5–89.0 Anteanal distance (aA) (mm) 44 135.1 ± 16.96 29 124.5 ± 11.25 105.0–156.5 111.0–153.0 Anteventral distance (aV)(mm) 4491.3±11.982985.1±7.99 69.0–107.5 75.0–105.0 Pectroventral distance (PV) (mm) 44 53.1 ± 6.63 29 49.0 ± 4.90 40.0–63.5 42.0–60.0 Ventroanal distance (VA) (mm) 44 45.8 ± 4.99 29 41.3 ± 3.67 35.0–53.0 35.3–50.0 Maximum body depth (H) (mm) 44 37.3 ± 4.09 29 34.6 ± 3.65 28.0–44.0 29.0–46.0 Caudal peduncle length (lCP) (mm) 44 28.5 ± 3.20 29 26.1 ± 2.23 21.0–34.0 21.5–32.0 Dorsal fin base length (lD) (mm) 44 19.2 ± 2.84 29 17.2 ± 2.24 13.0–24.0 10.5–21.0 Dorsal fin depth (hD) (mm) 44 31.1 ± 3.85 29 29.1 ± 2.92 21.5–38.5 25.0–35.0 Anal fin base length (lA) (mm) 44 23.4 ± 3.40 29 22.3 ± 2.67 14.0–31.0 17.0–27.0 Anal fin depth (hA) (mm) 44 21.3 ± 3.32 29 19.9 ± 2.31 13.0–30.0 16.0–25.0 Pelvic fin length (lV) (mm) 44 28.4 ± 3.75 29 26.2 ± 2.69 21.0–35.0 23.0–33.0 Pectoral fin length (lP) (mm) 44 30.5 ± 4.31 29 28.5 ± 3.17 21.5–37.0 24.0–34.0 Head length (C) (mm) 44 41.3 ± 5.39 29 38.6 ± 4.07 32.0–48.0 33.0–48.0

Head depth through the eye (hC1) (mm) 43 18.6 ± 2.64 29 17.4 ± 1.91 14.0–22.0 15.0–22.0

Head depth (at nape) (hC2) (mm) 44 25.2 ± 4.17 29 23.9 ± 2.74 17.5–31.5 18.0–30.0 Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula... 361

Table 3 (continued) Morphological characteristics Lineages

EALBP2

N M±σ N M±σ Min–max Min–max

Snout length (aO) (mm) 44 10.4 ± 1.31 29 10.1 ± 1.03 8.0–13.0 9.0–13.0 Horizontal diameter of eye (O) (mm) 44 10.6 ± 1.50 29 9.9 ± 1.16 8.0–13.0 8.5–13.0 Postorbital distance (pO) (mm) 44 21.3 ± 2.76 29 21.5 ± 1.09 16.5–25.0 17.9–24.5 Interorbital width (iO)(mm) 439.7±1.26298.2±1.01 7.0–12.0 6.5–11.0 Upper jaw (maxilla) length (lmx) (mm) 44 14.0 ± 1.89 29 12.9 ± 1.17 10.0–16.5 11.0–16.0 Lower jaw (mandible) length (lmd) (mm) 43 19.2 ± 2.57 29 17.4 ± 1.74 14.5–22.0 15.0–23.0

N is the number of fish in which the given character was analyzed; M is the mean value; σ is the standard deviation canonical variables. The majority of variation among groups differentiates the vendace of lineage E and specimens of the of vendace was explained by the first two canonical discrim- lakes Bol’shoye Krasnoye and Vishtynetskoye. These differ- inant functions (47.7% and 28.0%, respectively). All groups ences are explained by significant loadings of the most of were correctly classified with 100% accuracy. The first dis- body, head, and fin traits (Table 7). criminant function (Wilks’ λ = 0.00028; df = 115; p <0.000) The distribution of the samples in the space of the first two allows a clear separation vendace of Lake Beloye (Fig. 3). The discrimination functions reveals clear differentiation of vendace second function (Wilks’ λ = 0.00413; df = 88; p < 0.000) of Lake Beloye from other samples (Fig. 3). Surprisingly, the

Table 4 Significant differences in a comparison of median values of Population comparison Meristic traits meristic traits between different populations of C. albula of vt sp.br. Dub Db Aub Ab Pub Pb Vub Vb European north of Russia ALBP2 E ns SD SD ns ns ns ns ns ns ns ALBP2 B ns – ns SD ns SD ns ns ns ns ALBP2 V SD – ns SD SD ns ns ns ns ns ALBP2 BK –– ns ns ns ns ns ns ns ns ALBP2 G SD SD ns ns SD ns ns ns – ns EBns– ns SD ns SD ns ns ns ns EVSD– ns SD SD ns ns ns ns ns EBK–– SD SD ns ns ns ns ns ns E G SD SD ns ns ns SD ns ns – ns BK B –– ns SD ns SD ns SD ns ns BK V –– SD SD SD ns ns ns ns ns BK G –– ns SD ns ns ns ns – ns VBSD– ns SD SD SD ns ns ns ns VGSD– ns ns ns SD ns ns – ns GBSD– ns SD ns SD ns ns – ns

ALBP2 ALBP2 lineage of vendace of Lake Pleshcheyevo; E E lineage of vendace of Lake Pleshcheyevo; B Lake Beloye; V Lake Vishtynetskoye; BK Lake Bol’shoye Krasnoye; G Lake Goreloye SD Mann–Whitney U test significant at p <0.05;ns Mann–Whitney U test nonsignificant; B–^—the comparison was not carried out, since for one of the compared groups, there were no data on the trait 362 Borovikova E.A., Artamonova V.S.

Table 5 Fork length, Sm (mm), at age of vendace lineages of Lake Pleshcheyevo

Age (years) Sex Males Females Both males and females

Lineages Е ALBP2 E ALBP2 E ALBP2

2 n 6151112 M±σ 156.3 ± 8.04 157.0 159.2 ± 10.64 166.0 157.6 ± 8.94 161.5 Min–max 146–167 149–177 146–177 3 n 21525420 M±σ 191.0 175.2 ± 8.50 191.5 175.2 ± 16.52 191.3 ± 8.96 175.2 ± 9.87 Min–max 164–198 159–197 181–201 159–198 4 n 8113– 21 1 M±σ 197.6 ± 11.04 174.0 210.5 ± 3.69 – 205.6 ± 11.06 174.0 Min–max 176–207 206–216 176–216 5 n 1 – 6 – 7 – M±σ 195.0 – 209.2 ± 9.04 – 207.1 ± 9.84 – Min–max 201–225 195–225 6 n ––1313 M ––220.0 211.0 220.0 211.0 Min–max 207–215 207–215

M is the mean value; σ is the standard deviation; n is the number of fish of each age and sex groups

ALBP2 representatives are complete coincide with the vendace lineage are more differentiated from ALBP2 specimens than of Lake Goreloye (the Solovetsky Islands). The vendace of E vendace of the Solovetsky Archipelago. Despite this, the 95% confidence ellipses of two lineages of Lake Pleshcheyevo are Table 6 Correlations overlapped on DFA scatterplot. between discriminating Variables Root 1 variables and canonical discriminant functions aD 0.55 for E and ALBP2 pD 0.41 Discussion lineages of Lake aA 0.59 Pleshcheyevo aV 0.48 The data presented above convincingly demonstrate that both PV 0.36 phylogenetic lineages of vendace of Lake Pleshcheyevo be- VA 0.53 long to the species C. albula, because the variation ranges of H 0.29 their morphological characters either fall within the variation lCP 0.31 ranges characteristic of other populations of this species or lD 0.37 overlap with them. At the same time, very slight morpholog- hD 0.33 ical divergence revealed between individuals of the different lA 0.22 lineages can testify the importance of these traits for certain hA 0.27 ecologically relevant features of two lineages. lP 0.36 The two vendace lineages of Lake Pleshcheyevo signifi- cantly differ from each other in the number of gill rakers and lV 0.43 unbranched rays in dorsal fin (Tables 2 and 3). The difference C 0.64 of first trait suggests differences in feeding between the two hC 0.44 1 phylogenetic lineages. Obviously, the greater number of gill hC 0.43 2 rakers allow fish of lineage ALBP2 to feed on smaller zoo- pO 0.47 plankton organisms (Lazzaro 1987). The fins’ parameters are O 0.45 related to fish locomotion characteristics (Aleyev 1957; iO 0.51 Pokrovskii 1967; Pakkasmaa and Piironen 2000). Decrease aO 0.20 in the number of unbranched rays in the dorsal fin leads to a lmx 0.51 decrease in their surface area. This feature may indicate the lmd 0.61 different ability to moving in the water column and mobility of λ . % 100 E and ALBP2 specimens. λ is percentage of total variation. Observed morphological features of the E and ALBP2 lin- Significant correlations were not revealed eages allow suggesting that the different lineages should Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula... 363

Fig. 3 Plots of scores for the first two discriminant functions for size-free morphometric data for six vendace (C. albula)groups. 1—Lake Pleshcheyevo, lineage E; 2—Lake Pleshcheyevo, lineage ALBP2; 3—Lake Goreloye; 4—Lake Bol’shoye Krasnoye; 5—Lake Vishtynetskoye; 6—Lake Beloye. 95% confidence ellipses are shown

prefer different lake habitats, namely, the different depths or frequencies of alleles of some genes (Perelygin 1988). specific lake areas. However, long-term investigations did not Although lakes Ladoga and Pleshcheyevo considerably differ confirm this hypothesis: the preferences of certain localities in in size, several groups of vendace in them have formed in the lake were not revealed for specimens of the E and ALBP2 similar ways; in both cases, this is related to coexistence of lineages. Evidently, the representatives of the two lineages formerly allopatric groups in the same water body. form a single stock. Other example of sympatric populations of Coregonus,for There are published data that some morphological charac- which scenarios of allopatric divergence and introgression on ters of C. albula may vary with time as a result of changes in secondary contact are discussed, is the Baltic ciscoes the environmental conditions (Oreha and Skute 2009)orafter (Coregonus albula complex) from Germany lakes Stechlin introduction to a new water body (Sandlund 1992). At the and Breiter Luzin (Schulz et al. 2006;Mehneretal.2010). In same time, our data suggest that not only ecological, but also their case, morpho-ecological differentiation is more clearly other factors contribute to the observed differentiation of me- pronounced than for the vendace lineages of Lake ristic characters of the E and ALBP2 samples. One of these Pleshcheyevo: in the German lakes, autumn- and spring- factors can be different origin of two lineages of vendace of spawning ciscoes substantially differing by temperature- Lake Pleshcheyevo: two groups of fish inhabiting the same dependent metabolic adaptations coexist (Ohlberger et al. environmental conditions have strong different haplotypes of 2008a, b). At the same time, the data about genetic differentia- mtDNA (Borovikova 2017). tion between these sympatric populations are contradictory. It should be noted that Lake Pleshcheyevo is not the only Microsatellite loci revealed low levels of divergence for sym- water body where groups of vendace with distinctly differing patric pair of each lake. Moreover, Fst value for population pair morphological characters have been found. For example, the Lake Stechlin C. albula and C. fontanae was not significant. At small form of vendace of Lake Ladoga has been shown to be the same time, mtDNA polymorphism showed lower genetic differentiated into three stocks, each with its specific morpho- relatedness between sympatric taxa; all Fst and Фst p values logical and ecological characteristics (Dyatlov 1978). The au- were significant, except Фst value for comparison between thor explains the formation of these stocks by the geological Lake Stechlin C. albula and C. fontanae. Large-scale investi- history of the water body, which created conditions for long- gation of genetic differentiation of the sympatric groups of the term isolation of three groups of vendace during which they Baltic cisco using AFLP markers was performed by T. Mehner may have developed specific characteristics of morphology with co-authors (Mehner et al. 2010). The results of this study and mode of life. Later research in the polymorphism of failed to provide evidence for the mode of speciation of these protein-coding loci has shown that the local stocks of the small groups of fish, however indicate that multiple lineages may be form of vendace of Lake Ladoga differ from one another in the responsible for the complex patterns of Coregonus. 364 Borovikova E.A., Artamonova V.S.

Table 7 Correlations between discriminating variables and canonical and identifying the key factors that may affect fish morphol- discriminant functions for six samples of vendace (C. albula) of European ogy. At present on the data about mtDNA variability, we can north of Russia only discuss the meaning of different origins for morpholog- Variables Root 1 Root 2 ical difference of two lineages of Lake Pleshcheyevo. Separate analyses of the morphological characteristics of aD 0.48 − 0.43 two phylogenetic lineages of vendace living in the same water − pD 0.49*** 0.55*** body that have diverged from each other to the species level in − aA 0.50 0.47 terms of genetic parameters have led us to a generalization that − aV 0.49* 0.43* has a general biological significance: considerable genetic dif- − PV 0.39*** 0.32*** ferences between individuals do not necessarily mean that − VA 0.39 0.40 they belong to different species. The example of vendace of − H 0.09*** 0.43*** Lake Pleshcheyevo shows that long-term coexistence on the − lCP 0.41 0.38 same water body may lead to a situation where two genetically lD 0.21* − 0.52* different groups that have diverged from one another under hD 0.20 − 0.49 the conditions of allopatry, there is no hiatus between with lA 0.13 − 0.51 respect to many morphological parameters. In both groups, hA 0.16* − 0.51* most morphological characters vary within the intraspecific lP 0.40** − 0.35** variation ranges determined for populations that are unlikely lV 0.31** − 0.36** to be of polyphyletic origin. C 0.51** − 0.39** It is noteworthy that similar results were obtained in a study − hC1 0.28 0.44 on the polymorphism of the partial nucleotide sequence of the − hC2 0.21*** 0.60*** mitochondrial gene coI in North American freshwater fishes pO 0.43** − 0.43** by means of barcoding (April et al. 2011). The authors showed O 0.19*** − 0.38*** that a number of species contained intraspecific groups con- iO 0.23** − 0.54** siderably differentiated in terms of this nucleotide sequence aO 0.44*** − 0.08*** but insignificantly differing in morphology. In that study, it lmx 0.42** − 0.30** was assumed that these findings were related to allopatric lmd 0.45* − 0.25* origins and independent evolutionary histories of different in- λ, % 47.7 28.0 traspecific lineages. However, J. April with co-authors (April et al. 2011) did not mention any example of the coexistence of λ is percentage of total variation. Significance levels of correlations are genetically differentiated, but morphologically not distin- given as *p < 0.05, **p < 0.01, and ***p < 0.001 guished lineages in the same water body. This feature makes the vendace of Lake Pleshcheyevo the unique population of The testing of the two phylogenetic lineages of vendace of this species. Lake Pleshcheyevo for similarity with C. albula populations The case of Lake Pleshcheyevo vendace demonstrates that has yielded interesting findings. The first, the vendace of analysis of genetic characteristics of individuals, especially European part of Russia are morphologically heterogeneous. when based on limited number of genetic loci, is insufficient This species is characterized by vast variability of meristic and for classifying diverging groups as separate species. This morphological traits. The second, according to meristic and agrees with the conclusion made by April et al. (2011). In such morphometric data, the ALBP2 lineages of Lake cases, genetic analysis should be supported by study of the Pleshcheyevo are more closely related to vendace of the morphology of genetically differentiated groups and their oth- Solovetstky Archipelago lakes (Tables 2 and 4; Fig. 3). er biological characteristics. Of special importance is evidence In general, vendace, with their high ecological flexibility, for reproductive isolation of the groups. are characterized by rapid formation of specific morphological traits under specific environmental conditions, the resultant Acknowledgments We are grateful to M.Yu. Fedorov, director of the B ^ interpopulation differences being sometimes considerable National Park Lake Pleshcheyevo, as well as the personnel of the national park and our colleagues from IBIW RAS, for various help in (Borovikova et al. 2013; Delling et al. 2014). It should be collecting the material; Yulia V. Kodukhova and Nina V. Raushkina for noted that the contributions of the environmental and genetic the assistance in measurements; Alexei A. Bolotovski, Dmitri P. components to the formation of individual specific character- Karabanov, Alexander A. Makhrov, Mikhail I. Malin, and Alexei K. istics can only be estimated after detailed study of both mito- Smirnov for valuable comments and discussion of the manuscript. chondrial and nuclear genomes in representatives of the pop- Funding information The preparation of this manuscript was supported ulations included in each group, as well as analysis of the by the Russian Science Foundation, grant no. 16-14-10001. characteristics of water bodies inhabited by these populations Morphological specificities of vendace (Salmoniformes: Salmonidae: Coregoninae: Coregonus albula... 365

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