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Introgressive Hybridization between Southern Asian Dolly Varden, Salvelinus curilus, and Northern Dolly Varden, S. malma malma, on Sakhalin Island

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Abstract

Genetic characteristics of the southern Asian Dolly Varden, Salvelinus curilus, and northern Dolly Varden, S. malma malma, in northeastern Asia and the Aleutian Islands were examined using mitochondrial (mt) and microsatellite (ms) DNA markers. The maximum-likelihood tree based on mtDNA control region haplotypes showed two well-supported monophyletic lineages for these species, but the haplotypes found in the Sakhalin Island populations were an admixture of the two mtDNA lineages. Bayesian clustering using msDNA indicated that all individuals from Sakhalin Island grouped with the S. curilus populations, regardless of their mtDNA haplotype. Incongruence between mtDNA and msDNA markers provided strong evidence of historical mtDNA introgression from S. m. malma to S. curilus. Secondary contact by postglacial colonization from different refugia is a plausible explanation for the introgressive hybridization detected in Sakhalin Island.

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REFERENCES

  1. Avise, J.C., Phylogeography: The History and Formation of Species, London: Harvard University Press, 2000.

    Google Scholar 

  2. Hendry, A.P. and Stearns, S.C., Evolution Illuminated, Salmon and Their Relatives, New York: Oxford University Press, 2004.

    Google Scholar 

  3. Wilson, C.C. and Bernatchez, L., The ghost of hybrids past: fixation of arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush), Mol. Ecol., 1998, vol. 7, no. 1, pp. 127—132. https://doi.org/10.1046/j.1365-294x.1998.00302.x

    Article  Google Scholar 

  4. Redenbach, Z. and Taylor, E.B., Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America, Evolution, 2002, vol. 56, no. 5, pp. 1021—1035. https://doi.org/10.1554/0014-3820(2002)056[1021:EFHIAA]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  5. Radchenko, O.A., Introgressive hybridization of chars of the genus Salvelinus as inferred from mitochondrial DNA variation, Russ. J. Genet., 2004, vol. 40, no. 12, pp. 1678—1685. https://doi.org/10.1007/s11177-005-0068-y

    Article  CAS  Google Scholar 

  6. Yamamoto, S., Kitano, S., Maekawa, K., et al., Introgressive hybridization between Dolly Varden Salvelinus malma and white-spotted charr Salvelinus leucomaenis on Hokkaido Island, Japan, J. Fish Biol., 2006, vol. 68, suppl. A, pp. 68—85. https://doi.org/10.1111/j.0022-1112.2006.00994.x.

  7. Yamamoto, S., Morita, K., Kikko, T., et al., Phylogeography of a salmonid fish, masu salmon Oncorhynchus masou subspecies-complex, with disjunct distribution across the temperate northern Pacific, Freshw. Biol., 2020, vol. 65, no. 4, pp. 698—715. https://doi.org/10.1111/fweb.13460

    Article  CAS  Google Scholar 

  8. Barton, N.H. and Hewitt, G.M., Adaptation, speciation and hybrid zones, Nature, 1989, vol. 341, no. 6242, pp. 497—502. https://doi.org/10.1038/341497a0

    Article  CAS  PubMed  Google Scholar 

  9. Grant, P.R. and Grant, B.R., Hybridization of bird species, Science, 1992, vol. 256, no. 5054, pp. 193—197. https://doi.org/10.1126/science.256.5054.193

    Article  CAS  PubMed  Google Scholar 

  10. Taylor, E.B., Lowery, E., Lilliestråle, A., et al., Genetic analysis of sympatric char populations in western Alaska: Arctic char (Salvelinus alpinus) and Dolly Varden (Salvelinus malma) are not two sides of the same coin, J. Evol. Biol., 2008, vol. 21, no. 6, pp. 1609–1625. https://doi.org/10.1111/j.1420-9101.2008.01603.x

    Article  CAS  PubMed  Google Scholar 

  11. Gritsenko, O.F., Savvaitova, K.A., Gruzdeva, M.A., et al., On the taxonomic position of charr Salvelinus of the northern Kuril Islands, Vopr. Ikhtiol., 1998, vol. 38, no. 2, pp. 189—198.

    Google Scholar 

  12. Savvaitova, K.A., Gruzdeva, M.A., Kuzishchin, K.V., et al., Riverine charrs of the genus Salvelinus of the North Kuril Islands, Vopr. Ikhtiol., 2004, vol. 44, no. 1, pp. 89—101.

    Google Scholar 

  13. Dyldin, Yu.V. and Orlov, A.M., Ichthyofauna of fresh and brackish waters of Sakhalin Island: an annotated list with taxonomic comments: 2. Cyprinidae—Salmonidae families, J. Ichthyol., 2016, vol. 56, no. 5, pp. 656—693. https://doi.org/10.1134/S0032945216050040

    Article  Google Scholar 

  14. Yamamoto, S., Maekawa, K., Morita, K., et al., Phylogeography of the salmonid fish, Dolly Varden Salvelinus malma: multiple glacial refugia in the North Pacific Rim, Zool. Sci., 2014, vol. 31, no. 10, pp. 660—670. https://doi.org/10.2108/zs130266

    Article  Google Scholar 

  15. Oleinik, A.G., Skurikhina, L.A., Frolov, S.V., et al., Differences between two subspecies of Dolly Varden, Salvelinus malma, revealed by RFLP-PCR analysis of mitochondrial DNA, Environ. Biol. Fish., 2004, vol. 69, no. 1, pp. 449—459. https://doi.org/10.1023/B:EBFI.0000022897.26755.da

    Article  Google Scholar 

  16. Shedko, S.V., Ginatulina, L.K., Miroshnichenko, I.L., et al., Phylogeography of mitochondrial DNA in south Asian Dolly Varden char Salvelinus curilus Pallas, 1814 (Salmoniformes, Salmonidae): mediated gene introgression?, Russ. J. Genet., 2007, vol. 43, pp. no. 2, pp. 165—176. https://doi.org/10.1134/S1022795407020111.

  17. Osinov, A.G. and Mugue, N.S., Variation of the mitochondrial DNA control region in the populations of southern form of Dolly Varden (Salvelinus malma krascheninnikovi) from Sakhalin, Russ. J. Genet., 2008, vol. 44, no. 12, pp. 1668—1676. https://doi.org/10.1134/S1022795408120090

    Article  CAS  Google Scholar 

  18. Frolov, S.V., Frolova, V.N., and Molodichenko, A.V., Karyotype of the char Salvelinus malma of the Yama River (Magadan oblast) and taxonomical status of the northern and the southern chars, Russ. J. Mar. Biol., 1997, vol. 23, pp. 269—272.

    Google Scholar 

  19. Phillips, R.B., Gudex, L.I., Westrich, K.M., et al., Combined phylogenetic analysis of ribosomal ITS1 sequences and new chromosome data supports three subgroups of Dolly Varden char (Salvelinus malma), Can. J. Fish. Aquat. Sci., 1999, vol. 56, no. 8, pp. 1504—1511. https://doi.org/10.1139/f99-103

    Article  CAS  Google Scholar 

  20. Balakirev, E.S., Romanov, N.S., and Ayala, F.J., Complete mitochondrial genomes of the northern (Salvelinus malma) and southern (Salvelinus curilus) Dolly Varden chars (Salmoniformes, Salmonidae), Mitochondrial DNA, Part A, 2016, vol. 27, no. 2, pp. 1016—1017. https://doi.org/10.3109/19401736.2014.926531

    Article  CAS  Google Scholar 

  21. Oleinik, A.G., Skurikhinba, L.A., and Brykov, Vl.A., Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data, Russ. J. Genet., 2015, vol. 51, no. 1, pp. 55—68. https://doi.org/10.1134/S1022795415010093

    Article  CAS  Google Scholar 

  22. Salmenkova, E.A., Omelchenko, V.T., Kolesnikov, A.A., et al., Genetic differentiation of chars in the Russian north and far east, J. Fish Biol., 2000, vol. 57, suppl. A, pp. 136—157. https://doi.org/10.1111/j.1095-8649.2000.tb02250.x.

  23. Salmenkova, E.A. and Omelchenko, V.T., Genetic divergence and taxonomic status of chars of the genus Salvelinus, Biol. Bull. Rev., 2013, vol. 3, pp. 481—492. https://doi.org/10.1134/S2079086413060078

    Article  Google Scholar 

  24. Uiblein, F., Jagsch, A., Honsig-Erlenburg, W., et al., Status, habitat use, and vulnerability of the European grayling in Austrian waters, J. Fish Biol., 2001, vol. 59, suppl. A, pp. 223—247. https://doi.org/10.1111/j.1095-8649.2001.tb01388.x.

  25. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, pp. 4673—4680. https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Brunner, P.C., Douglas, M.R., Osinov, A., et al., Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences, Evolution, 2001, vol. 55, no. 3, pp. 573—586. https://doi.org/10.1554/0014-3820(2001)055[0573:hpo-acs]2.0.co;2

    Article  CAS  PubMed  Google Scholar 

  27. Yamamoto, S. and Sekino, M., Isolation and characterization of tri- and tetra-repeat microsatellite loci in the white-spotted charr Salvelinus leucomaenis (Salmonidae), J. Fish Biol., 2015, vol. 86, no. 3, pp. 1199—1202. https://doi.org/10.1111/jfb.12628

    Article  CAS  PubMed  Google Scholar 

  28. Dehaan, P.W. and Ardren, W.R., Characterization of 20 highly variable tetranucleotide microsatellite loci for bull trout (Salvelinus confluentus) and cross-amplification in other Salvelinus species, Mol. Ecol. Notes, 2005, vol. 5, no. 3, pp. 582—585. https://doi.org/10.1111/j.1471-8286.2005.00997.x

    Article  CAS  Google Scholar 

  29. Angers, B., Bernatchez, L., Angers, A., et al., Specific microsatellite loci for brook charr reveal strong population subdivision on a microgeographic scale, J. Fish Biol., 1995, vol. 47, pp. 177—185. https://doi.org/10.1111/j.1095-8649.1995tb06054.x

    Article  CAS  Google Scholar 

  30. O’Reilly, P.T., Hamilton, L.C., McConnell, et al., Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites, Can. J. Fish. Aquat. Sci., 1996, vol. 53, no. 10, pp. 2292—2298. https://doi.org/10.1139/f96-192

    Article  Google Scholar 

  31. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870—1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Goudet, J., FSTAT ver. 2.9.3.2, Lausanne: University of Lausanne, 2002.

    Google Scholar 

  33. Excoffier, L. and Lischer, H.E.L., Arlequin Suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, no. 3, pp. 564—567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  34. Rice, W.R., Analyzing tables of statistical tests, Evolution, 1989, vol. 43, no. 1, pp. 223—225. https://doi.org/10.1111/j.1558-5646.1989.tb04220.x

    Article  PubMed  Google Scholar 

  35. Pritchard, J.K., Stephens, M., and Donnelly, P., Inference of population structure using multilocus genotype data, Genetics, 2000, vol. 155, no. 2, pp. 945—959.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Evanno, G., Regnaut, S., and Goudet, J., Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study, Mol. Ecol., 2005, vol. 14, no. 8, pp. 2611—2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  37. Li, Y.L. and Liu, J.X., StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods, Mol. Ecol. Resour., 2018, vol. 18, no. 1, pp. 176—177. https://doi.org/10.1111/1755-0998.12719

    Article  PubMed  Google Scholar 

  38. Felsenstein, J., PHYLIP (Phylogeny Inference Package) version 3.695, Seattle, WA: Department of Genome Science, University of Washington, 2004. https://doi.org/10.1002/9780471650126.dob0534.pub2

  39. Peakall, R. and Smouse, P.E., GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update, Bioinformatics, 2012, vol. 28, no. 19, pp. 2537—2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Phillips, R.B., Sajdak, S.L., and Domanico, M.J., Relationships among charrs based on DNA sequences, Nord. J. Freshw. Res., 1995, vol. 71, pp. 378—391.

    Google Scholar 

  41. Oleinik, A. G., Skurikhina, L.A., Brykov, V.A., et al., Differentiation of Dolly Varden char Salvelinus malma from Asia and North America inferred from PCR-RFLP analysis of mitochondrial DNA, Russ. J. Genet., 2005, vol. 41, no. 5, pp. 501—508. https://doi.org/10.1007/s11177-005-0118-5

    Article  CAS  Google Scholar 

  42. Dunham, J., Baxter, C., Fausch, K., et al., Evolution, ecology, and conservation of Dolly Varden, white-spotted char, and bull trout. Fisheries, 2008, vol. 33, pp. 537—550. https://doi.org/10.1577/1548-8446-33.11.537

    Article  Google Scholar 

  43. Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Divergence of the Salvelinus species mitochondrial DNA from northeastern Asia, Ecol. Freshw. Fish., 2007, vol. 16, no 1, pp. 87—98. https://doi.org/10.1111/j.1600-0633.2006.00187.x

    Article  Google Scholar 

  44. Oleinik, A.G., Skurikhina, L.A., Bondar, E.I., et al., Phylogeography of northern Dolly Varden Salvelinus malma malma based on analysis of mitochondrial DNA, J. Zool. Syst. Evol. Res., 2014, vol. 52, no 4, pp. 293—304. https://doi.org/10.1111/jzs.12067

    Article  Google Scholar 

  45. Gordeeva, N.V., Chukova, E.I., and Oleinik, A.G., Microsatellite genetic variation of Asian populations of Dolly Varden char, Hydrobiologia, 2010, vol. 650, vol. 1, pp. 133—144. https://doi.org/10.1007/s10750-010-0104-3.

  46. Toews, D.P.L. and Brelsford, A., The biogeography of mitochondrial and nuclear discordance in animals, Mol. Ecol., 2012, vol. 21, no. 16, pp. 3907—3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x

    Article  CAS  PubMed  Google Scholar 

  47. Wirtz, P., Mother species-father species: unidirectional hybridization in animals with female choice, Anim. Behav., 1999, vol. 58, no. 1, pp. 1—12. https://doi.org/10.1006/anbe.1999.1144

    Article  CAS  PubMed  Google Scholar 

  48. Kitano, S., Size-related factors causing individual variation in seasonal reproductive success of fluvial male Dolly Varden (Salvelinus malma), Ecol. Freshw. Fish, 1996, vol. 5, pp. 59—67. https://doi.org/10.1111/j.1600-0633.1996.tb00037.x

    Article  Google Scholar 

  49. Kishi, D., and Maekawa, K., Stream-dwelling Dolly Varden (Salvelinus malma) density and habitat characteristics in stream sections installed with low-head dams in the Shiretoko Peninsula, Hokkaido, Japan, Ecol. Res., 2009, vol. 24, no. 4, pp. 873—880. https://doi.org/10.1007/s11284-008-0562-5

    Article  Google Scholar 

  50. DeCicco, A., Long-distance movements of anadromous Dolly Varden between Alaska and the USSR, Arctic, 1992, vol. 45, no. 2, pp. 120—123. https://www. jstor.org/stable/40511213.

    Article  Google Scholar 

  51. Maekawa, K. and Nakano, S., Latitudinal trends in adult body size of Dolly Varden, with special reference to the food availability hypothesis, Popul. Ecol., 2002, vol. 44, no. 1, pp. 17—22. https://doi.org/10.1007/s101440200002

    Article  Google Scholar 

  52. Morita, K., Morita, S., Furukawa, M., et al., Offshore Dolly Varden charr (Salvelinus malma) in the North Pacific, Environ. Biol. Fish., 2009, vol. 86, no. 4, pp. 451—456. https://doi.org/10.1007/s10641-009-9547-7

    Article  Google Scholar 

  53. Baxter, J.S., Taylor, E.B., Devlin, R.H., et al., Evidence for natural hybridization between Dolly Varden (Salvelinus malma) and bull trout (Salvelinus confluentus) in a north central British Columbia watershed, Can. J. Fish. Aquat. Sci., 1997, vol. 54, no. 2, pp. 421—429. https://doi.org/10.1139/cjfas-54-2-421

    Article  Google Scholar 

  54. Kitano, S., Maekawa, K., Nakano, S., et al., Spawning behavior of bull trout in the upper Flathead drainage, Montana, with special reference to hybridization with brook trout, Trans. Amer. Fish. Soc., 1994, vol. 123, no. 6, pp. 988—992. https://doi.org/10.1577/1548-8659(1994)123<0988:NS-BOBT>2.3.CO;2

    Article  Google Scholar 

  55. Ostberg, C.O., Slatton, S.L., and Rodriguez, R.J., Spatial partitioning and asymmetric hybridization among sympatric coastal steelhead trout (Oncorhynchus mykiss), coastal cutthroat trout (O. clarki clarki) and interspecific hybrids, Mol. Ecol., 2004, vol. 13, no. 9, pp. 2773—2788. https://doi.org/10.1111/j.1365-294X.2004.02268.x

    Article  CAS  PubMed  Google Scholar 

  56. Kitano, S., Ohdachi, S., Koizumi, I., et al., Hybridization between native white-spotted charr and non-native brook trout in the upper Sorachgi River, Hokkaido, Japan, Ichthyol. Res., 2014, vol. 61, pp. 1—8. https://doi.org/10.1007/s10228-013-0362-y

    Article  Google Scholar 

  57. Fukui, S., May-McNally, S. L., Taylor, E. B., et al., Maladaptive secondary sexual characteristics reduce the reproductive success of hybrids between native and non-native salmonids, Ecol. Evol., 2018, vol. 8, no. 23, pp. 12173—12182. https://doi.org/10.1002/ece3.4676

    Article  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to Maki Yoshida, Atsuko Yada, and Shima Matsunaga for assistance with genetic analysis. We also thank Katsutoshi Watanabe for helpful discussion and comments.

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This study was supported by JSPS KAKENHI grant number 16K07884.

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Yamamoto, S., Morita, K., Sahashi, G. et al. Introgressive Hybridization between Southern Asian Dolly Varden, Salvelinus curilus, and Northern Dolly Varden, S. malma malma, on Sakhalin Island. Russ J Genet 57, 361–370 (2021). https://doi.org/10.1134/S1022795421030145

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