Abstract
Arctic rainbow smelt Osmerus dentex is one of the most abundant fish species widely distributed in the NW Pacific and Arctic seas. Studying this species can contribute to understanding the microevolutionary processes of the Arctic fauna in unstable climatic conditions and new habitats. However, little is known about the genetic structure and the mechanisms underlying its population dynamics. Ten microsatellite loci were used to genotype 822 individuals in 20 locations throughout a large part of the species’ range in the Sea of Japan, Sea of Okhotsk, Bering, Kara, and White seas (across more than 11,000 km). O. dentex displayed substantial levels of genetic differentiation (overall FST = 0.067, RST = 0.091) and STRUCTURE identified eight distinct clusters. The significant regional variation was demonstrated in both genetic diversity and population structure, most notably between Arctic and Pacific basins. On a regional scale, contrasting patterns were revealed with limited gene flow between populations of the Arctic region (FST = 0.117) and high gene flow between the Bering Sea (FST = 0.017) or Sea of Okhotsk (FST = 0.031), which were probably associated with differences in larval distribution from the spawning grounds due to different oceanographic conditions of the studied areas. These results demonstrate the effect of local contemporary forces in sha** different patterns of genetic connectivity and diversity within O. dentex.
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Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, Malden
Allendorf FW, Ryman N, Utter F (1987) Genetics and fishery management. In: Ryman N, Utter F (eds) Population genetics and fisheries management. University of Washington Press, Seattle and London, pp 1–19
Altukhov KA, Yerastova VM (1974) Biological characteristics of smelt, Osmerus eperlanus L. from Karelian White Sea coast. J Ichthyol 14:67–78
Andriashev AP, Chernova NV (1994) Annotated list of fishlike vertebrates and fish of the Arctic seas and adjacent waters. J Ichthyol 35:81–123
Baby MC, Bernatchez L, Dodson JJ (1991) Genetic structure and relationships among anadromous and landlocked populations of rainbow smelt, Osmerus mordax, Mitchill, as revealed by mtDNA restriction analysis. J Fish Biol 39:61–68
Beacham TD, Hay DE, Le KD (2005) Population structure and stock identification of eulachon (Thaleichthys pacificus), an anadromous smelt, in the Pacific Northwest. Mar Biotechnol 7:363–372
Berg LS (1948) Freshwater fishes of the USSR and adjacent countries. Akademiya Nauk SSSR, Moscow-Leningrad (in Russian)
Berger VY (2007) Production Potential of the White Sea. St. Petersburg Zoological Institute RAS, Saint-Petersburg (in Russian)
Bernatchez L, Martin S (1996) Mitochondrial DNA diversity in anadromous rainbow smelt, Osmerus mordax Mitchill: a genetic assessment of the member-vagrant hypothesis. Can J Fish Aquat Sci 53:424–433
Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452
Bradbury IR, Coulson MW, Campana SE, Bentzen P (2006) Morphological and genetic differentiation in anadromous smelt Osmerus mordax (Mitchill): disentangling the effects of geography and morphology on gene flow. J Fish Biol 69:95–114
Bradbury IR, Campana SE, Bentzen P (2008a) Low genetic connectivity in an estuarine fish with pelagic larvae. Can J Fish Aquat Sci 65:147–158
Bradbury IR, Campana SE, Bentzen P (2008b) Estimating contemporary early life-history dispersal in an estuarine fish: integrating molecular and otolith elemental approaches. Mol Ecol 17:1438–1450
Bradbury IR, Coulson MW, Campana SE et al (2011) Contemporary nuclear and mitochondrial genetic clines in a north temperate estuarine fish reflect Pleistocene vicariance. Mar Ecol Prog Ser 438:207–218
Bugaev AV (2007) The fish of the Kamchatka River watershed. Kamchatpress, Petropavlovsk-Kamchatsky (in Russian)
Bugaev AV, Amelchenko YuN, Lipnyagov SV (2014) Rainbow smelt Osmerus mordax dentex in the shelf zone and inland water bodies of Kamchatka: state of stock, fishery, and biological structure. Izv TINRO 178:3–24 (in Russian)
Burlak OV (2018) Research of the Azian smelt Osmerus mordax in the Amur river basin in 2017. Prospects for fisheries and aquaculture in the modern world, p 66 (in Russian)
Chereshnev IA (1998) Biogeography of freshwater fishes of far east of Russia. Dal’nauka, Vladivostok (in Russian)
Chereshnev IA, Volobuev VV, Shestakov AV, Frolov SV (2002) Salmonoid fishes in Russian north-east. Dal’nauka, Vladivostok (in Russian)
Chernyavsky VI (1981) Circulation systems in the Sea of Okhotsk. Russian Proc TINRO 105:13–19
Costello AB, Down TE, Pollard SM et al (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344
Coulson MW, Paterson IG, Green A et al (2006) Characterization of di- and tetranucleotide microsatellite markers in rainbow smelt (Osmerus mordax). Mol Ecol Res 6:942–944
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
Dodson JJ, Tremblay S, Colombani F et al (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Mol Ecol 16:5030–5043
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and experimental considerations. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, Amsterdam, pp 55–86
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Evseenko SA, Mishin AV (2011) On the distribution of larvae and localization of spawning stocks of White Sea herring Clupea pallasii marisalbi. J Ichthyol 51:776–787
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Filatov NN, Nazarova LE, Druzhinin PV (2019) Influence of climatic and anthropogenic factors of the White Sea-catchment system. Proc KNT RAS 9:30–50. https://doi.org/10.17076/lim1117
Fisch KM, Petersen JL, Baerwald MR et al (2009) Characterization of 24 microsatellite loci in delta smelt, Hypomesus transpacificus, and their cross-species amplification in two other smelt species of the Osmeridae family. Mol Ecol Res 9:405–408
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Gladenkov AY, Gladenkov YB (2004) Onset of connections between the Pacific and Arctic Oceans through the Bering Strait in the Neogene. Stratigr Geol Correl 12:175–187
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html
Grioche A, Koubbi P (1997) A preliminary study of the influence of a coastal frontal structure on ichthyoplankton assemblages in the English Channel. ICES J Mar Sci 54:93–104
Gritsenko OF (2002) Diadromous fishes of Sakhalin (systematics, ecology, fisheries). VNIRO, Moscow (in Russian)
Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hardy OJ, Charbonnel N, Freville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482
Hutchinson DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914
Iles TD, Sinclair M (1982) Atlantic herring: stock discreteness and abundance. Science 215:627–633
Jenkins DG, Carey M, Czerniewska J et al (2010) A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33:315–320
Jensen JL, Bohonak AJ, Kelley ST 2005. Isolation by distance, web service. BMC Genet 6:13. http://ibdws.sdsu.edu/
Kaukinen KH, Supernault KJ, Miller KM (2004) Development of microsatellite loci in eulachon (Thaleichthys pacificus). Mol Ecol Res 4:632–634
Khen GV, Ustinova EI, Sorokin Y (2019) Principal climate indices for the North Pacific: nature and history (a review). Russian Proc TINRO 197:166–181
Kirpichnikov VS (1935) Biological and systematic essay on smelt of the White Sea, Czech Bay, and Pechora River. Tr. VNIRO 2:103–191 (in Russian)
Klyukanov VA (1975) The status of Osmeridae in the system of order Salmoniformes. J Ichthyol 15:3–20
Kobylyanskii SG, Drits AV, Mishin AV et al (2014) Small scale distribution of the White Sea herring larvae (Clupea pallasii marisalbi) in relation to hydrophysical features. Oceanology 54:752–762
Koizumi I, Yamamoto S, Maekawa K (2006) Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr. Mol Ecol 15:3175–3189
Kopelman NM, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191
Koskinen MT, Nilsson J, Veselov AJ et al (2002) Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae. Heredity 88:391–401
Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat Cornol and Freyhof, Berlin
Kovach AI, Breton TS, Enterline C, Berlinsky DL (2013) Identifying the spatial scale of population structure in anadromous rainbow smelt (Osmerus mordax). Fish Res 141:95–106
Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data: Version 1.0 (d 16c). http://lewis.eeb.unconn.edu/lewishome/software.html
Lu G, Basley DJ, Bernatchez L (2001) Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Mol Ecol 10:965–985
Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm.” Human Biol 76(2):173–190
McCauley DE (1993) Genetic consequences of extinction and recolonization in fragmented habitats. In: Kareiva PM, Kingsolver JG, Huey RB (eds) Biotic interactions and global change. Sinauer Associates, Sunderland, pp 217–233
McLean J, Taylor E (2001) Resolution of population structure in a species with high gene flow: microsatellite variation in the eulachon (Osmeridae: Thaleichthys pacificus). Mar Biol 139:411–420
Munk P, Larsson PO, Danielssen DS, Moksness E (1999) Variability in frontal zone formation and distribution of gadoid fish larvae at the shelf break in the northeastern North Sea. Mar Ecol Prog Ser 177:221–233
Naumova TN, Kolomeitsev VV (2015) Some data about biology and distribution of larval capelin (Mallotus villosus catervarius) on the shelf of west Kamchatka. Issled Vodn Biol Resur Kamchat Sev-Zap Chasti Tikhogo Okeana 38:84–92 (in Russian)
Nellbring S (1989) The ecology of smelts (genus Osmerus): a literature review. Nord J Freshw Res 65:116–145
Pantyulin AN (2003) Hydrological system of the White Sea. Oceanology 43:1–14
Pantyulin AN (2012) Dynamics, structure, and water masses. In: Lisitzin AP (ed) The White Sea system. Water column and interacting atmosphere, cryosphere, river flow and biosphere. Nauchnyi Mir, Moscow, pp 309–379 (in Russian)
Parukhina LV (2009) Summer ichthyoplankton of the Dvina Bay of the White Sea. In: Proceedings of the XXVIII international conference on biological resources of the White Sea and Inland Reservoirs of European North, KNT RAS, Petrozavodsk, pp 407–411 (in Russian)
Parukhina LV (2016) Abundance and some features of biology of smelt Osmerus mordax dentex larvae in the Onega Bay of the White Sea. In: Proceedings of the conference on marine biological research: achievements and perspectives, ECOSI-Hydrophisic, Sevastopol, pp 239–241 (in Russian)
Peterson DP, Ardren WR (2009) Ancestry, population structure, and conservation genetics of Arctic grayling (Thymallus arcticus) in the upper Missouri River, USA. Can J Fish Aquat Sci 66:1758–1774
Piry S, Luikart G, Conuet JM (1999) Bottleneck: a computer program for detecting recent reduction in the effective population size using allele frequency data. J Hered 90:502–503
Podushko YN (1970) Biological characteristic of the rainbow smelt Osmerus eperlanus dentex Steindachner in Lower Amur. Izv. TINRO 74:130–138 (in Russian)
Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Sabates A, Olivar MP (1996) Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar Ecol Prog Ser 135:11–20
Saint-Laurent R, Legault M, Bernatchez L (2003) Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Mol Ecol 12:315–330
Semenova AV, Stroganov AN, Afanas’ev KI, Rubtsova GA (2015) Population structure and variability of Pacific herring (Clupea pallasii) in the White Sea, Barents and Kara Seas revealed by microsatellite DNA analyses. Polar Biol 38:951–965
Semenova AV, Stroganov AN, Ponomareva EV, Afanas’ev KI (2019a) Microsatellite variability of the Arctic rainbow smelt Osmerus dentex from the White Sea. Russ J Genet 55:770–772
Semenova AV, Stroganov AN, Bugaev AV et al (2019b) An analysis of microsatellite polymorphism in the population of the Arctic rainbow smelt Osmerus dentex from Eastern and Western Kamchatka. Russ J Genet 55:77–88
Sendek DS, Studenov II, Sherstkov VS et al (2005) Genetic differentiation among smelt fish of the genus Osmerus (Osmeridae, Salmoniformes) in the European North of Russia. In: Salmonid fishes of eastern Fennoscandia. Karelsk Nauch Tsentr Ross Akad Nauk, Petrozavodsk, pp 148–157 (in Russian)
Skurikhina LA, Oleinik AG, Kukhlevsky AD et al (2015) Genetic differentiation of Pacific smelt Osmerus mordax dentex inferred from the data of mitochondrial DNA analysis. Rus J Genet 51:1221–1232
Skurikhina LA, Oleinik AG, Kukhlevsky AD et al (2018) Phylogeography and demographic history of the Pacific smelt Osmerus dentex inferred from mitochondrial DNA variation. Polar Biol 41:877–896
Skurikhina LA, Oleinik AG, Kukhlevsky AD et al (2019) Molecular genetic analysis of the relationships and origin of smelt (Hypomesus, Osmeridae), a new component of the fauna of the Barents Sea. Rus J Genet 55:1082–1092
Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Stamford MD, Taylor EB (2004) Phylogeographical lineages of Arctic grayling (Thymallus arcticus) in North America: divergence, origins and affinities with Eurasian Thymallus. Mol Ecol 13:1533–1549
Stasenkov VA, Studenov II, Novoselov AP et al (2011) Pomor fisheries. Pravda Severa, Arkhangelsk ([in Russia])
Taylor EB, Dodson JJ (1994) A molecular analysis of relationships and biogeography within a species complex of Holarctic fish (genus Osmerus). Mol Ecol 3:235–248
Tonteri A, Titov S, Veselov A et al (2005) Phylogeography of anadromous and non-anadromous Atlantic salmon (Salmo salar) from northern Europe. Ann Zool Fennici 42:1–22
Ulchenko VA, Matkovskiy AK, Stepanov SI et al (2016) Fish resources and their development in the estuaries of the Kara Sea and the Laptev Sea. Proc VNIRO 160:116–132 (in Russian)
Vähä J-P, Erkinaro J, Niemelä E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genoty** errors in microsatellite data. Mol Ecol Notes 4:535–538
Varkentin AI, Buslov AV, Tepnin OB (2001) Some features of spawning and distribution of pollock eggs in the waters of Western Kamchatka. Proc TINRO 128:177–187 (in Russian)
Vasilets PM (2000) On scale structure and growth rate of the Pacific smelt Osmerus mordax dentex (Osmeridae) from the Kamchatka waters during the first two years of life. J Ichthyol 40:397–401
Vasilets PM, Trofimov IK, Raevskii RV (2000) Morphological differentiation of Rainbow Smelt, Osmerus mordax dentex Kamchatka Waters. Tr. KamchatNIRO 5:101–105 (in Russian)
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Ye J, Coulouris G, Zaretskaya I et al (2012) PrimerBLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134
Zhivotovsky LA (1991) Population biometrics. Nauka, Moscow (in Russian)
Acknowledgements
The reported study was funded by Russian Foundation for Basic Research, Project Number 19-04-00244-a. The use of DNA markers for population differentiation was supported by the Russian Science Foundation No. 19-16-00101. The work was also carried out within the framework of the state theme GZ 0112-2019-0002 (sub-topic ‘Ecological and genetic structure of the species’).We are grateful to Alla N. Gorbacheva and Edward V. Golzha for their help in samples collection. We thank the Editor in Chief, Dieter Piepenburg, and the three reviewers Niall McKeown, Cristian B. Canales-Aguirre, and Vidar Wennevik for their valuable comments on an earlier draft of this manuscript.
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AVS performed and designed research, analysed data, and wrote the manuscript. EP and OV conducted field work. ANS and KA provided research opportunity. All authors read and approved the manuscript.
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Semenova, A.V., Stroganov, A.N., Ponomareva, E.V. et al. Large-scale genetic structure and diversity of Arctic rainbow smelt Osmerus dentex Steindachner et Kner, 1870 throughout its distributional range based on microsatellites. Polar Biol 44, 927–940 (2021). https://doi.org/10.1007/s00300-021-02848-x
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DOI: https://doi.org/10.1007/s00300-021-02848-x