Abstract
El’gygytgyn is the only ancient lake in the Arctic that avoided continental-scale glaciations. This lake is located on an arid mountain plateau, far from the main routes of post-glacial freshwater fish dispersal, and it is therefore challenging to consider the local fauna in a historical context. Here we present a study of the ecology and evolutionary history of the local charr complex (genus Salvelinus). We found that the endemic charrs exhibit extreme longevity, contrasting lifestyles and phenotypes. Salvelinus svetovidovi is a relic benthivorous species. The remaining charrs are descendants of Salvelinus taranetzi. Mitochondrial and microsatellite DNA polymorphisms analyzed in them and in charrs from surrounding basins indicate that S. taranetzi invaded the lake from Arctic Chukotka in the late Pleistocene as two distinct, previously diverged lineages. Descendants of both lineages occupied the pelagic food chain. The first lineage has flourished as a monomorphic planktivorous population since colonization. The second represents an example of a recent in-lake adaptive divergence, in which a deepwater piscivore specialist formed a new epilimnetic ecomorph of an impressive size (up to 9.0 kg). We suggest that this diversification was triggered by modern warming in the Arctic, which led to the formation of a productive littoral ecosystem.
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References
ACIA. 2004. Impacts of a warming arctic-arctic climate impact assessment. In Hassol, S. (ed.), Cambridge University Press, Cambridge
Albrecht, C. & T. Wilke, 2008. Ancient Lake Ohrid: biodiversity and evolution. Hydrobiologia 615: 103–140. https://doi.org/10.1007/s10750-008-9558-y.
Alekseyev, S. S., V. P. Samusenok, A. N. Matveev & MYu. Pichugin, 2002. Diversification, sympatric speciation and trophic polymorphism of Arctic charr, Salvelinus alpinus complex in Transbaikalia. Environmental Biology of Fishes 64: 97–114. https://doi.org/10.1007/978-94-017-1352-8_8.
Amundsen, P.-A., H.-M. Gabler & F. J. Staldvik, 1996. A new approach to graphical analyses of feeding strategy from stomach contents data: modification of the Costello (1990) method. Journal of Fish Biology 48: 607–614. https://doi.org/10.1111/j.1095-8649.1996.tb01455.x.
Anderson, P. H. & A. V. Lozhkin, 2001. The Stage 3 interstadial complex (Karginskii/middle Wisconsinan interval) of Beringia: Variations in paleoenvironments and implications for paleoclimatic interpretations. Quaternary Science Reviews 20: 93–125. https://doi.org/10.1016/S0277-3791(00)00129-3.
Beaumont, M. A., W. Zhang & D. J. Balding, 2002. Approximate Bayesian computation in population genetics. Genetics 162: 2025–2035. https://doi.org/10.1093/genetics/162.4.2025.
Brunner, P. C., M. R. Douglas, A. Osinov, C. C. Wilson & L. Bernatchez, 2001. Holarctic phylogeography of Arctic charr (Salvelinus alpinus L) inferred from mitochondrial DNA sequences. Evolution 55(3): 573–586. https://doi.org/10.1554/0014-3820(2001)055[0573:hpoacs]2.0.co;2.
Chavarie, L., K. L. Howland & W. M. Tonn, 2013. Sympatric polymorphism in Lake trout: the coexistence of multiple shallow-water morphotypes in Great Bear Lake. Transections of the American Fisheries Society 142: 814–823. https://doi.org/10.1080/00028487.2013.763855.
Chereshnev, I. A. & M. B. Skopets, 1990. Salvethymus svetovidovi gen. et sp. nova: a new endemic fish of the subfamily Salmoninae from Lake El’gygytgyn (Central Chukotka). Voprosy Ikhtiologii 30(2): 201–213 ((in Russian)).
Chereshnev, I. A., V. V. Volobuev, A. V. Shestakov & S. V. Frolov, 2002. Salmonid fishes in Russian North-East, Dal’nauka Press, Vladivostok: ((in Russian)).
Chereshnev, I. A. 2008. Freshwater fishes of Chukotka, Far-Eastern Branch of RUS, Magadan: ((in Russian)).
Cornuet, J.-M., P. Pudlo, J. Veyssier, A. Dehne-Garcia & A. Estoup, 2014. DIYABC v20: a software to make Approximate Bayesian Computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30(8): 1187–1189. https://doi.org/10.1093/bioinformatics/btt763.
Cristescu, M. E., S. J. Adamowicz, J. J. Vaillant & D. G. Haffner, 2010. Ancient lakes revisited: from the ecology to the genetics of speciation. Molecular Ecology 19: 4837–4851. https://doi.org/10.1111/j.1365-294X.2010.04832.x.
DeHaan, P. W. & W. R. Ardren, 2005. Characterization of 20 highly variable tetranucleotide microsatellite loci for Bull trout (Salvelinus confluentus) and cross-amplification in other Salvelinus species. Molecular Ecology Notes 5: 582–585. https://doi.org/10.1111/j.1471-8286.2005.00997.x.
Dryden, I. L. & K. V. Mardia, 1998. Statistical Shape Analysis, Wiley, Chichester:
Earl, D. A. & B. M. vonHoldt, 2012. Structure Harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4(2): 359–361. https://doi.org/10.1007/s12686-011-9548-7.
Esin, E. V., E. S. Bocharova, E. A. Borisova & G. N. Markevich, 2020. Interaction among morphological, trophic and genetic groups in the rapidly radiating Salvelinus fishes from Lake Kronotskoe. Evolutionary Ecology 34: 611–632. https://doi.org/10.1007/s10682-020-10048-y.
Esin, E. V., G. N. Markevich, D. V. Zlenko & F. N. Shkil, 2021. Thyroid-mediated metabolic differences underlie ecological specialization of extremophile salmonids in the Arctic Lake El’gygytgyn. Frontiers in Ecology and Evolution 9: 715110. https://doi.org/10.3389/fevo.2021.715110.
Esin, E. V., N. O. Melnik, L. A. Pelgunova & G. N. Markevich, 2022. Probing for depth-gradient diversification in the riverine-spawning Dolly Varden: Insights from a recently discovered ecomorph assemblage. Ecology of Freshwater Fish 32(2): 322–335. https://doi.org/10.1111/EFF.12688.
Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software Structure: A simulation study. Molecular Ecology 14: 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x.
Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.
Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925. https://doi.org/10.1093/genetics/147.2.915.
Garza, J. C. & E. G. Williamson, 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10: 305–318. https://doi.org/10.1046/j.1365-294x.2001.01190.x.
Glushkova, OYu., 2011. Late Pleistocene glaciations in north-east Asia. Developments in Quaternary Sciences 15: 865–875. https://doi.org/10.1016/B978-0-444-53447-7.00063-5.
Gordeeva, N. V., A. G. Osinov, S. S. Alekseyev, A. N. Matveev & V. P. Samusenok, 2010. Genetic differentiation of Arctic charr Salvelinus alpinus complex from Transbaikalia revealed by microsatellite markers. Journal of Ichthyology 50: 351–361. https://doi.org/10.1134/S0032945210050012.
Grainger, E. H., 1953. On the age, growth, migration, reproductive potential and feeding habitats of the Arctic charr (Salvelinus alpinus) of Frobisher bay, Baffin Island. Journal of the Fisheries Research Board of Canada 10: 326–370.
Gusakov, V. A., V. G. Gagarin, F. N. Shkil & D. V. Zlenko, 2022. Eudorylaimus chukotkanus sp. n. and E mylnikovi sp. n. (Nematoda: Dorylaimida) from Lake El’gygytgyn (Chukotka, Russia). Inland Water Biology 15(2): 97–106. https://doi.org/10.1134/S1995082922020055.
Hall, T., 2011. BioEdit: an important software for molecular biology. GERF Bulletin of Biosciences 2(1): 60–61.
Heino, J., J. M. Culp & Erkinaro, J, Goedkoop, W., & J. P. Smol, 2020. Abruptly and irreversibly changing Arctic freshwaters urgently require standardized monitoring. Journal of Applied Ecology 57(7): 1192–1198. https://doi.org/10.1111/1365-2664.13645.
Hirano, T., T. Saito, Y. Tsunamoto, J. Koseki & S. Chiba, 2019. Role of ancient lakes in genetic and phenotypic diversification of freshwater snails. Molecular Ecology 28(23): 5032–5051. https://doi.org/10.1111/mec.15272.
Janes, J. K., J. M. Miller, J. R. Dupuis, R. M. Malenfant & R. L. Andrew, 2017. The K= 2 conundrum. Molecular Ecology 26(14): 3594–3602. https://doi.org/10.1111/mec.14187.
Jonsson, B. & N. Jonsson, 2001. Polymorphism and speciation in Arctic charr. Journal of Fish Biology 58: 605–638. https://doi.org/10.1111/j.1095-8649.2001.tb00518.x.
Kharitonov, V. G. & S. I. Genkal, 2010. Centric diatom algae (Centrophyceae) of ultraoligotrophic Lake Elgygytgyn and water bodies of its basin (Chukotka, Russia). Inland Water Biology 3(1): 1–10. https://doi.org/10.1134/S1995082910010013.
Klingenberg, C. P., 2008. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11(2): 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.
Klingenberg, C. P. & L. R. Monteiro, 2005. Distances and directions in multidimensional shape spaces: implications for morphometric applications. Systematic Biology 54(4): 678–688. https://doi.org/10.1080/10635150590947258.
Knudsen, R. & A. Klemetsen, 1994. Infections of Diphyllobothrium dendriticum, D. ditremum (Cestoda), and Cystidicola farionis (Nematoda) in a north Norwegian population of Arctic charr (Salvelinus alpinus) during winter. Canadian Journal of Zoology 72(11): 1922–1930. https://doi.org/10.1139/z94-261.
Knudsen, R., A. Siwertsson, C. Adams, M. Garduno-Paz & P.-A. Amundsen, 2011. Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures. Evolutionary Ecology 25: 589–604. https://doi.org/10.1007/s10682-010-9451-9.
Koval, M. V., E. V. Esin, S. L. Gorin, R. S. Galyamov & V. E. Koshel, 2018. Fish species diversity, distribution, and dispersal in the rivers of the Penzhina Bay catchment area. Journal of Ichthyology 58(6): 795–807. https://doi.org/10.1134/S0032945218050119.
Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev/msy096.
Kundyshev, A. S. & N. B. Verkhovskaya, 1984. Drainage network development in the upper Anadyr drainage basin. Geomorfologiya 4: 68–73.
Kuzmina, S. A., A. V. Sher, M. E. Edwards, J. Haile & E. Willerslev, 2011. The late Pleistocene environment of the Eastern West Beringia based on the principal section at the Main River, Chukotka. Quaternary Science Reviews 30: 2091–2106. https://doi.org/10.1016/j.quascirev.2010.03.019.
Leigh, J. W. & D. Bryant, 2015. POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution 6(9): 1110–1116. https://doi.org/10.1111/2041-422210X.12410.
Luethje, M. & J. Snyder, 2021. Climate-related morphological changes in Pantocsekiella (Mediophyceae) spanning 0–1.2 Ma in the Lake Elgygytgyn, northeastern Russia including Pantocsekiella elgygytgynensis sp. nov. Phytotaxa 478(1): 67–91. https://doi.org/10.11646/phytotaxa.478.1.5.
Markevich, G. N., M. M. Solovyev, P. G. Vlasenko, G. V. Izotova & E. V. Esin, 2023. Phylogeny, distribution, and biology of Pygmy whitefish (Prosopium coulterii) in the Beringia Region (Chukotka). Diversity 15(4): 547. https://doi.org/10.3390/d15040547.
Melles, M., J. Brigham-Grette, P. S. Minyuk, N. R. Nowaczyk & B. Wagner, 2012. 2.8 Million years of Arctic climate change from Lake El’gygytgyn NE Russia. Science 337(6092): 315–320. https://doi.org/10.1126/science.1222135.
Nolan, M., E. N. Cassano & J. J. Cassano, 2013. Synoptic climatology and recent climate trends at Lake El’gygytgyn. Climate of the past 9: 1271–1286. https://doi.org/10.5194/cp-9-1271-2013.
Oleinik, A. G., E. I. Bondar, A. D. Kukhlevsky, L. A. Skurikhina & N. E. Kovpak, 2021. Introgressive hybridization between two phylogenetic lineages of charrs (Salvelinus: Salmonidae) in northeastern Asia. Journal of Zoological Systematics and Evolutionary Research 59(8): 2119–2133. https://doi.org/10.1111/jzs.12563.
Osinov, A. G., A. L. Senchukova, N. S. Mugue, S. D. Pavlov & I. A. Chereshnev, 2015. Speciation and genetic divergence of three species of charr from ancient Lake El’gygytgyn (Chukotka) and their phylogenetic relationships with other representatives of the genus Salvelinus. Biological Journal of the Linnean Society 116(1): 63–85. https://doi.org/10.1111/bij.12559.
Osinov, A. G. & A. A. Volkov, 2020. On the origin of two species of charrs (Salvelinus, Salmonidae) in Lake El’gygytgyn: Data on the ATPase6-NADH4L region of mitochondrial DNA. Journal of Ichthyology 60(4): 618–625. https://doi.org/10.1134/S003294522004013X.
Osinov, A. G., A. A. Volkov & D. A. Pavlov, 2022. Secondary contact, hybridization, and diversification in Arctic charr (Salvelinus alpinus (L). species complex) from lakes of the Norilo-Pyasinskaya water system, Taimyr: how many forms exist there? Hydrobiologia 849(11): 2521–2547. https://doi.org/10.1007/s10750-022-04869-x.
Peakall, R. & P. E. Smouse, 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28: 2537–2539. https://doi.org/10.1093/bioinformatics/bts460.
Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology 18: 293–320. https://doi.org/10.1146/annurev.es.18.110187.001453.
Piggott, C. V. H., E. Verspoor, R. Greer, O. Hooker, J. Newton & C. E. Adams, 2018. Phenotypic and resource use partitioning amongst sympatric, lacustrine brown trout, Salmo trutta. Biological Journal of the Linnean Society 20: 200–212. https://doi.org/10.1093/biolinnean/bly032.
Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi & C. G. Montana, 2007. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189. https://doi.org/10.1007/s00442-006-0630-x.
Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959. https://doi.org/10.1093/genetics/155.2.945.
Radchenko, O. A., 2003. Variability of mitochondrial DNA in populations of lake charrs from genus Salvelinus in the Far East and Siberia. Journal of Ichthyology 43: 539–547.
Rohlf, F. J., 2015. The Tps series of software. Hystrix 26(1): 9–12. https://doi.org/10.4404/hystrix-26.1-11264.
Rossiterm, A. & H. Kawanabe, 2000. Ancient lakes: biodiversity, ecology and evolution. Advances in Ecological Research 31: 624.
Rouse, W. R., M. S. Douglas, R. E. Hecky, A. E. Hershey & J. P. Smol, 1998. Effects of climate change on the freshwaters of arctic and subarctic North America. Hydrological Processes 11(8): 873–902.
Rousset, F., 2008. Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x.
Rozas, J., A. Ferrer-Mata, J. C. Sánchez-DelBarrio, S. Guirao-Rico & A. Sánchez-Gracia, 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34(12): 3299–3302. https://doi.org/10.1093/molbev/msx248.
Salmenkova, E. A., V. T. Omelchenko, K. I. Afanasyev, G. A. Rubtsova & MYu. Kovalev, 2009. Genetic divergence of populations of the white char Salvelinus albus, Northern and Southern forms of malma S malma (Salmonidae), by microsatellite loci of DNA. Journal of Ichthyology 49(9): 730–740. https://doi.org/10.1134/S0032945209090045.
Tabata, R., R. Kakioka, K. Tominaga, T. Komiya & K. Watanabe, 2016. Phylogeny and historical demography of endemic fishes in Lake Biwa: the ancient lake as a promoter of evolution and diversification of freshwater fishes in western Japan. Ecology and Evolution 6(8): 2601–2623. https://doi.org/10.1002/ece3.2070.
Takezaki, N., M. Nei & K. Tamura, 2014. POPTREEW: web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Molecular Biology and Evolution 31(6): 1622–1624. https://doi.org/10.1093/molbev/msu093.
Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023.
Thompson, J. D., T. J. Gibson & D. G. Higgins, 2003. Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics 1(2): 3. https://doi.org/10.1002/0471250953.bi0203s00.
Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x.
Vander Zanden, M. J., S. Chandra, S. Park, Y. Vadeboncoeur & C. R. Goldman, 2006. Efficiencies of benthic and pelagic trophic pathways in a subalpine lake. Canadian Journal of Fisheries and Aquatic Sciences 63: 2608–2620. https://doi.org/10.1139/f06-148.
Zelditch, M. L., D. L. Swiderski, H. D. Sheets & W. L. Fink, 2004. Geometric morphometrics for biologists: a primer, Elsevier Academic Press, New York:
Zimmerman, M. S., C. C. Krueger & R. L. Eshenroder, 2007. Morphological and ecological differences between shallow- and deep-water Lake trout in Lake Mistassini, Quebec. Journal of Great Lakes Research 33: 156–169. https://doi.org/10.3394/0380-1330(2007)33[156:MAEDBS]2.0.CO;2.
Acknowledgements
The authors express their deep gratitude to Evgeny G. Rudnev, the inspirer and participant of the work in the Arctic. The study was conducted in frame of the IEE RAS and IDB RAS research programs nos. 0089-2021-0003 and 0088-2021-0019, respectively.
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Esin, E.V., Shkil, F.N., Zlenko, D.V. et al. Quaternary history and radiation of Salvelinus fish in the ancient Arctic Lake El’gygytgyn. Hydrobiologia 851, 2389–2404 (2024). https://doi.org/10.1007/s10750-023-05464-4
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DOI: https://doi.org/10.1007/s10750-023-05464-4