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Phylogeography of Littorina sitkana in the northwestern Pacific Ocean: evidence of eastward trans-Pacific colonization after the Last Glacial Maximum

Abstract

We investigated genetic diversity and population structure of the Sitka periwinkle Littorina sitkana along the coastlines of the northwestern Pacific (NWP) to evaluate the possibility of trans-Pacific colonization of this species from the NWP to the northeastern Pacific (NEP) after the Last Glacial Maximum. We sampled L. sitkana from 32 populations in the NWP, and sequenced a region of the mitochondrial cytochrome b oxidase gene for population genetic analyses. The results were compared with those of previous reports from the NEP. The genetic diversity of L. sitkana was much higher in the NWP than in the NEP. Genetic connectivity between the NWP and NEP populations was indicated by an extremely abundant haplotype in the NEP that was also present in eastern Hokkaido and the Kuril Islands. To confirm these results, we compared sequences of the longest intron of the aminopeptidase N gene (APN54) in the nuclear genome in four populations of L. sitkana in the NWP with previous results from the NEP. Again, much higher genetic diversity was found in the NWP than in the NEP and genetic connectivity was supported between the Kuril Islands and the NEP. These results imply postglacial colonization of this species from the NWP to the NEP, probably along the Kuril and Aleutian Island chains. This study is the first report of possible trans-Pacific postglacial colonization of a direct-developing gastropod, inferred from genetic data.

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References

  • Azuma N, Yamazaki T, Chiba S (2011) Mitochondrial and nuclear DNA analysis revealed a cryptic species and genetic introgression in Littorina sitkana (Mollusca, Gastropoda). Genetica 139 (11–12):1399–1408

    CAS  Article  PubMed  Google Scholar 

  • Behrens Yamada S (1977) Geographic range limitation of the intertidal gastropods Littorina sitkana and L. planaxis. Mar Biol 39:61–65

    Article  Google Scholar 

  • Botta AM, Rochette R, Saunders GW, Addison JA, Barbeau MA (2014) Evidence for genotypic differentiation between marine snails (Littorina sitkana) from the upper- and lower-intertidal zone in Bamfield Inlet (British Columbia, Canada). J Exp Mar Biol Ecol 461:389–396

    Article  Google Scholar 

  • Buckland-Nicks JA, Chia F-S (1990) Egg capsule formation and hatching in the marine snail Littorina sitkana. Philos T Roy Soc B 326:159–176

    Article  Google Scholar 

  • Buckland-Nicks JA, Chia F-S, Behrens S (1973) Oviposition and development of two intertidal snails, Littorina sitkana and Littorina scutulata. Can J Zoolog 51:359–365

    Article  Google Scholar 

  • Canino MF, Spies IB, Cunningham KM, Hauser L, Grant WS (2010) Multiple ice-age refugia in Pacific cod, Gadus macrocephalus. Mol Ecol 19:4339–4351

    Article  PubMed  Google Scholar 

  • Cassone BJ, Boulding EG (2006) Genetic structure and phylogeography of lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts. Mar Biol 149:213–226. doi:10.1007/s00227-005-0197-9

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    CAS  Article  PubMed  Google Scholar 

  • Cox LN, Zaslavskaya NI, Marko PB (2014) Phylogeography and trans-Pacific divergence of the rocky shore gastropod Nucella lima. J Biogeogr 41:615–627. doi:10.1111/jbi.12217

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • 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. doi:10.1111/j.1755-0998.2010.02847.x

    CAS  PubMed  PubMed Central  Google Scholar 

  • Favorite F, Dodimead AJ, Nasu K (1976) Oceanography of the Subarctic Pacific region, 1960–71. Bull 33. International North Pacific Fisheries Commission, Vancouver. http://www.npafc.org/new/inpfc/INPFC%20Bulletin/Bull%20No.33/Bulletin%2033.pdf

  • Gordillo S, Nielsen SN (2013) The Australasian muricid gastropod Lepsiellaas Pleistocene visitor to southernmost South America. Acta Palaeontol Pol 58:777–783. doi:10.4202/app.2011.0186

    Google Scholar 

  • Gutow L, Beermann J, Buschbaum C, Rivadeneira MM, Thiel M (2015) Castaways can’t be choosers—homogenization of rafting assemblages on floating seaweeds. J Sea Res 95:161–171. doi:10.1016/j.seares.2014.07.005

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hasegawa K (2000) Family Littorinidae. In: Okutani T (ed) Marine Mollusks in Japan. Tokai University Press, Tokyo, pp 137–143

    Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol Jour Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1111/j.1095-8312.1999.tb01160.x

    CAS  Article  PubMed  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans Biol Sci 359:183–195. doi:10.1098/rstb.2003.1388

    CAS  Article  Google Scholar 

  • Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima Current into the Sea of Japan between 3.5 and 0.8 Ma. Palaeo 236(3):355–366

    Google Scholar 

  • Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845. doi:10.1007/s002270000412

    CAS  Article  Google Scholar 

  • Lambeck K, Rouby H, Purcell A, Sun Y, Sambridge M (2014) Sea level and global ice volumes from the Last Glacial Maximum to the Holocene. Proc Nat Acad Sci 111:15296–15303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Lee HJ, Boulding EG (2009) Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol Ecol 18:2165–2184. doi:10.1111/j.1365-294X.2009.04169.x

    CAS  Article  PubMed  Google Scholar 

  • Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck and Schlegel, 1845). Mol Ecol 16:275–288. doi:10.1111/j.1365-294X.2006.03140.x

    CAS  Article  PubMed  Google Scholar 

  • Marko PB, Hoffman JM, Emme SA, Mcgovern TM, Keever C, Cox LM (2010) The expansion-contraction model of Pleistocene demography: rocky shores suffer a sea change? Mol Ecol 19:146–169. doi:10.1111/j.1365-294X.2009.04417.x

    CAS  Article  PubMed  Google Scholar 

  • Nikula R, Fraser CI, Spencer HG, Waters JM (2010) Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Mar Ecol Prog Ser 40:221–230

    Article  Google Scholar 

  • Nohara M (1999) Genetic and conchologicl variation in Littorina sitkana Philippi (Mollusca, Gastropoda) on Northern Japanese Coasts. Zool Sci 16:309–317

    Article  Google Scholar 

  • Ohgaki S (1983) Distribution of the family Littorinidae (Gastropoda) in Hokkaido, with special emphasis on the distribution in Akkeshi Bay. Nankiseibutu 25:173–180 (in Japanese)

    Google Scholar 

  • Ohshima KI, Wakatsuchi M, Fukamachi Y (2002) Near-surface circulation and tidal currents of the Okhotsk Sea observed with satellite-tracked drifters. J Geophys Res 107:3195. doi:10.1029/2001JC001005

    Article  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571. doi:10.1016/j.tree.2008.06.010

    Article  PubMed  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0

    Google Scholar 

  • Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, London

  • Reid DG, Dyal P, Williams ST (2012) A global molecular phylogeny of 147 periwinkle species (Gastropoda Littorininae). Zool Scr 41:125–136. doi:10.1111/j.1463-6409.2011.00505.x

    Article  Google Scholar 

  • Sato S, Kojima H, Ando J, Ando H, Wilmot RL, Seeb LW et al (2004) Genetic population structure of chum salmon in the Pacific Rim inferred from mitochondrial DNA sequence variation. Environ Biol Fish 69:37–50. doi:10.1023/B:EBFI.0000022881.90237.aa

    Article  Google Scholar 

  • Sokolova IM, Boulding EG (2004) Length polymorphisms in an intron of Aminopeptidase N provide a useful nuclear DNA marker for Littorina species (Caenogastropoda). J Moll Stud 70:165–172

    Article  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    CAS  Article  PubMed  Google Scholar 

  • Thiel M, Gutow L (2005) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr. Mar Biol 43:279–418

    Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution Int J org Evolution 55:2455–2469

    CAS  Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution Int J org Evolution 38:1358–1370. doi:10.2307/2408641

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zaslavskaya NI, Pudovkin (2005) Macrogeographic genetic variability in the gastropod mollusk Littorina sitkana from Northewest Pacific. Rus J Genet 41:291–300

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank Prof. H. Takahashi of The Hokkaido University Museum and Dr A. A. Taran of the Sakhalin Branch of the Botanical Garden-Institute, Far Eastern Branch, Russian Academy of Sciences, for their kind help in sample collection and for their logistic support. We thank Dr Vl. A. Brykov and Dr A. V. Chernyshev of A. V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, for helping to collect samples. The authors gratefully acknowledge Dr D. G. Reid for the English language review. This study was supported by a Grant-in-Aid for Advanced Study Projects from Tokyo University of Agriculture.

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Correspondence to Noriko Azuma.

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Azuma, N., Zaslavskaya, N.I., Yamazaki, T. et al. Phylogeography of Littorina sitkana in the northwestern Pacific Ocean: evidence of eastward trans-Pacific colonization after the Last Glacial Maximum. Genetica 145, 139–149 (2017). https://doi.org/10.1007/s10709-017-9952-3

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Keywords

  • Trans-Pacific
  • Gastropod
  • Postglacial colonization
  • Sitka periwinkle