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European grayling (Thymallus thymallus) mtDNA control region haplotypes diversity and postglacial colonization of Russian European North

Ekaterina Ponomareva1*, Aleksandr Volkov2, Mariia Ponomareva1, Galina Makeenko3 and Elena Shubina4
  • 1 Department of Biology, Lomonosov Moscow State University, Russia
  • 2 All-Russian Research Institute Fisheries and Oceanography, Russia
  • 3 Knipovich Polar Research Institute of Marine Fisheries and Oceanography, Russia
  • 4 Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Russia

In recent years the scientific interest to European grayling (T. thymallus) has become rather high, nevertheless in the Russian part of the areal most of the populations still remain unexplored, the data are fragmentary and relate only to some rivers. At the same time, it should be noted that a great advantage for genetic studies of grayling in Russian European North is the populations natural environment such as low anthropogenic influence and absence of translocations. In addition, the features of this species – freshwater, stenohaline, not making long migrations – make the grayling a good object for phylogeographical studies and allow to reconstruct ways of colonization after glacial retreat. Accordingly, the objective of our study was to clarify the phylogenetic position of the European grayling on the territory of Russian European North. In addition, another objective was to clarify the relatedness of the Arctic grayling haplotype mtDNA revealed by Koskinen et al., 2000 in the sample of European grayling from the Syamzhenga River (the Northern Dvina basin). A total of 249 fish from 29 locations from the Kola Peninsula to the Urals were analyzed, 223 of them were European graylings and 26 were Arctic graylings (T. arcticus) from lakes of the Ob’ River (Subpolar Urals). Control region (CR) mtDNA amplification were performed by protocols as Weiss et al., 2002. Multiple alignment of sequences and phylogenetic analyzes were performed in the Geneious® 6.0.5 program (Biomatters Ltd.). Trees constructed in MrBayes 3.2.6. (Huelsenbeck, Ronquist, 2001), chain length 1 100 000. Deposited in the GenBank® (NCBI) CR mtDNA nucleotide sequences were used for dendrograms construction and named as Ca (Marić et al., 2014), At (Weiss et al., 2002), Gog, Edy, Ole (Weiss et al., 2006). 1046 bp mtDNA fragment including complete CR sequence was analyzed. 36 haplotypes (including indel) were identified, 32 haplotypes were described for the first time. Examined haplotypes of European graylings formed three clusters (Fig.1). The haplotype designated by us as "Main" or its variants differing by 1-2 substitutions were found in most of samples eastwards from the Onega Lake, and formed "Northern Russian" cluster. In contrast, in samples from the rivers of the Kola Peninsula and the Onega Lake there were haplotypes differing from the "Main" by five or more substitutions and they formed "Scandinavian" cluster. Haplotypes from the Ilych tributary of the Pechora river formed third group, forming one cluster with "Caspian" haplotypes (Marić et al., 2014). Two haplotypes of Arctic grayling were identified in the sample from the Vyya, eastern tributary of the Northern Dvina, one of them corresponded to the Sja05 previously revealed by Koskinen et al., 2000, Weiss et al., 2006. Also, in two samples from Kola Peninsula – in the Umba river and the Lake Seydozero – all analyzed haplotypes belonged to the Arctic grayling. A total of 11 haplotypes with indels were detected in the Umba and Seydozero samples. It is surprising that in all studied graylings from these samples (about 50 in total) no haplotypes of European grayling were revealed. Analyzed haplotypes of Arctic grayling from Ob’ samples formed two clusters, differing by 5-6 substitutions (Fig. 2). Four haplotypes from the Ob’ basin lakes formed an independent cluster, whereas the haplotypes of the European grayling samples clustered with one of the haplotypes of the Arctic grayling from the Ob’ basin (Subpolar Ural). Thus, the Russian part of European grayling areal is inhabited by three maternal lineages: "Scandinavian", "Northern Russian" and "Caspian". "Scandinavian" lineage has common origin with Baltic basin populations. Geographical distribution of haplotypes allows to suppose the existence of a common refugium with Baltic basin populations, from where European grayling could spread over Eastern Fennoscandia, the Kola Peninsula and to some tributaries of the Northern Dvina, and "Northern Russian" lineage originated from refugium which presumably existed in the Pechora Proglacial lake from where European grayling could spread to the eastern and northeastern rivers of European Russia. This is supported by the distributions of haplotypes and that "Main" haplotype was spread with a high frequency in samples from waterbodies situated to the east of the Northern Dvina. Discovered haplotypes of Arctic grayling in the samples of European grayling may indicate the existence of the Arctic grayling paleoareal on the territory of the European Arctic coast, and the postglacial introgression of the European grayling to the territory formerly inhabited by the Arctic grayling. As a result of paleoclimatic changes, the fragmentation of Arctic grayling areal took place, the species could survive only in certain refugia, and hybridization with European grayling could have occurred due to lack of spawners. It seems that the presence and moreover the high diversity of Arctic grayling haplotypes in fishes from waterbodies on the Kola Peninsula suggest the existence of a refugium in the Khibiny Mountains during glacial periods. Fig.1. Subtree of CR haplotypes (HKY85 substitution model) of European grayling constructed from MrBayes 3.2.6. (chain length 1 100 000). The posterior probabilities are indicated in the tree nodes. Haplotypes obtained in our work are designated bold letters and colours, Main – the most common haplotype. Fig. 2. Subtree of CR haplotypes (HKY85 substitution model) of Arctic grayling constructed from MrBayes 3.2.6. (chain length 1 100 000). The posterior probabilities are indicated in the tree nodes. Haplotypes obtained in our work are designated bold letters and colours.

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Acknowledgements

We express our gratitude for the help in collecting the material to Amosov A.P., Gordeeva N.V., Kulakova A.N., Pakhov I.I., Vedernikov Yu.G.

References

Huelsenbeck, J.P., Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 (8), 754-755. Koskinen, M.T., Ranta, E., Piironen, J., Veselov, A., Titov, S., Haugen, T.O., Nilsson, J., Carlstein, M., Primmer, C.R. (2000). Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Mol. Ecol. 9, 1609–1624. Marić, S., Askeyev, I.V., Askeyev, O.V., Monakhov, S.P., Bravničar, J., Snoj, A. (2014). Phylogenetic and population genetic analysis of Thymallus thymallus (Actinopterigii, Salmonidae) from the middle Volga and upper Ural drainages. Hydrobiologia 70 (1), 167–176. Weiss, S., Persat, H., Eppe, R., Schlötterer, C., Uiblein, F. (2002). Complex patterns of colonization and refugia revealed for European grayling Thymallus thymallus, based on complete sequencing of the mitochondrial DNA control region. Mol. Ecol. 11, 1393–1407. Weiss, S., Knizhin, I., Kirillov, A., Froufe, E. (2006). Phenotypic and genetic differentiation of two major phylogeographical lineages of arctic grayling Thymallus arcticus in the Lena River, and surrounding Arctic drainages. Biol. J. Linn. Soc. Lond. 88 (4), 511-525.

Keywords: Thymallus thymallus, Thymallus arcticus, Control region (CR), Postglacial colonization, Russian European North, Introgressive hybridization

Conference: XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019.

Presentation Type: Oral

Topic: GRAYLING (GENUS THYMALLUS): EVOLUTION, SYSTEMATICS, MANAGEMENT AND CONSERVATION

Citation: Ponomareva E, Volkov A, Ponomareva M, Makeenko G and Shubina E (2019). European grayling (Thymallus thymallus) mtDNA control region haplotypes diversity and postglacial colonization of Russian European North. Front. Mar. Sci. Conference Abstract: XVI European Congress of Ichthyology. doi: 10.3389/conf.fmars.2019.07.00068

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Received: 08 May 2019; Published Online: 14 Aug 2019.

* Correspondence: Mx. Ekaterina Ponomareva, Department of Biology, Lomonosov Moscow State University, Moscow, Russia, kponom@mail.ru