Advertisement

Mytilus trossulus in NW Greenland is genetically more similar to North Pacific than NW Atlantic populations of the species

  • Lis Bach
  • Malgorzata Zbawicka
  • Jakob Strand
  • Roman Wenne
Short Communication

Abstract

Changes in climate-related factors such as ice coverage, water temperature, and ocean currents have been proposed to facilitate an increased interchange of species in the High Arctic between the Pacific and Atlantic oceans. In Greenland, the colonization of the mussel species Mytilus edulis has been suggested to have occurred recently and exclusively from Northwest Atlantic populations. The source population for its sibling species Mytilus trossulus is however unknown, and therefore we aimed to explore its genetic origin. Using 54 SNP markers, M. trossulus was identified from three Greenland blue mussel populations collected in 2012–2014 and the relative similarities to Northwest Atlantic and North Pacific M. trossulus populations were assessed. Populations were found to fall into two clades. The North Pacific is the most likely source for the northern Greenland M. trossulus probably as a result of occasional postglacial long-distance dispersal through the Bering Strait.

Our findings in M. trossulus are in agreements with the predictions that climate change will, in addition to driving a northward expansion of temperate-boreal species into the Arctic Ocean, increase the rate of trans-Arctic interchange between the Atlantic and the Pacific oceans.

Keywords

Biogeography Trans-Arctic transportation SNPs Mytilus edulis Mytilus trossulus Greenland 

Notes

Acknowledgements

The authors gratefully acknowledge Anders Mosbech and Rune Dietz for sampling of mussels at Savissivik in northwestern Greenland, and Dr. Peter Cranford for providing samples from Canada. We thank Jonathan Gardner and Jean-Pierre Desforges for valuable comments on the manuscript.

Funding information

This study was partially funded by the 2011/01/B/NZ9/04352 NCN project for R.W., the Leading National Research Centre (KNOW) - the Centre for Polar Studies for the period 2014–2018 and statutory topic IV.1. in the IOPAS. L.B. received financial support from the Ministry of Environment and Food of Denmark.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Supplementary material

12526_2018_870_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 13 kb)
12526_2018_870_MOESM2_ESM.docx (17 kb)
ESM 2 (DOCX 17 kb)
12526_2018_870_MOESM3_ESM.docx (27 kb)
ESM 3 (DOCX 27 kb)
12526_2018_870_MOESM4_ESM.txt (60 kb)
ESM 4 (TXT 59 kb)
12526_2018_870_MOESM5_ESM.docx (16 kb)
ESM 5 (DOCX 15 kb)

References

  1. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. (2003) GENETIX version 4.04, logiciel sous Windows™ pour la genetique des populations. Laboratoire Genome, Populations, Interactions: CNRS UMR 5000, Université de Montpellier II, MontpellierGoogle Scholar
  2. Bennike O, Wagner B (2013) Holocene range of Mytilus edulis in central East Greenland. Polar Rec 49:291–296CrossRefGoogle Scholar
  3. Benzécri JP (1992) Correspondence analysis handbook. In: Balakrishnan N, Schucany WR, Garvey PR (eds) Statistics: a series of textbooks and monographs, Vol 125. Marcel Dekker, New York, NYGoogle Scholar
  4. Berge J, Johnsen G, Nilsen F, Gulliksen B, Slagstad D (2005) Ocean temperature oscillations enable reappearance of blue mussels Mytilus edulis in Svalbard after a 1000 year absence. Mar Ecol Prog Ser 303:167–175CrossRefGoogle Scholar
  5. De Schepper S, Schreck M, Beck KM, Matthiessen J, Fahl K, Mangerud G (2015) Early Pliocene onset of modern Nordic Seas circulation related to ocean gateway changes. Nat Commun 6:8659CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dyke AS, Dale JE, McNeely RN (1996) Marine mollusks as indicators of environmental change in glaciated North America and Greenland during the last 18000 years. Géog Phys Quatern 50(2):125–184Google Scholar
  7. Feder HM, Norton DW, Geller JB (2003) A review of apparent 20th century changes in the presence of mussels (Mytilus trossulus) and macroalgae in Arctic Alaska, and of historical and paleontological evidence used to relate mollusc distributions to climate change. Arctic 56(4):391–407CrossRefGoogle Scholar
  8. Fraïsse C, Belkhir K, Welch JJ, Bierne N (2016) Local interspecies introgression is the main cause of extreme levels of intraspecific differentiation in mussels. Mol Ecol 25:269–286CrossRefPubMedGoogle Scholar
  9. Gabriel S, Ziaugra L, Tabbaa D (2009) SNP genotyping using the Sequenom MassARRAY iPLEX platform. Curr Protoc Hum Genet 60:2.12.1–12.12.18Google Scholar
  10. Gardner JPA, Zbawicka M, Westfall KM, Wenne R (2016) Invasive blue mussels threaten regional scale genetic diversity in mainland and remote offshore locations: the need for baseline data and enhanced protection in the Southern Ocean. Glob Chang Biol 22:3182−3195.Google Scholar
  11. Helmuth B, Mieszkowska N, Moore P, Hawkins SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu Rev Ecol Evol Syst 37:373–404CrossRefGoogle Scholar
  12. Hoarau G, Rijnsdorp AD, Van Der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176CrossRefPubMedGoogle Scholar
  13. Høpner Petersen G (1978) Life cycles and population dynamics of marine benthic bivalves from the Disko Bugt area of West Greenland. Ophelia 17:95–120CrossRefGoogle Scholar
  14. Larrain MA, Zbawicka M, Araneda C, Gardner JPA, Wenne R (2018) Native and invasive taxa on the Pacific coast of South America: Impacts on aquaculture, traceability and biodiversity of blue mussels (Mytilus spp.). Evol Appl 11:298–311.Google Scholar
  15. Mathiesen SS, Thyrring J, Hemmer-Hansen J, Berge J, Sukhotin A, Leopold P, Bekaert M, Sejr MK, Nielsen EE (2017) Genetic diversity and connectivity within Mytilus spp. in the subarctic and Arctic. Evol Appl 10(1):39–55CrossRefPubMedGoogle Scholar
  16. Nelson RJ, Carmack EC, McLaughlin FA, Cooper GA (2009) Penetration of Pacific zooplankton into the western Arctic Ocean tracked with molecular population genetics. Mar Ecol Prog Ser 381:129–138CrossRefGoogle Scholar
  17. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354CrossRefPubMedGoogle Scholar
  18. Piry S (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefPubMedGoogle Scholar
  19. Rannala B, Mountain JL (1997) Detecting immigration using multilocus genotypes. Proc Natl Acad Sci U S A 94:9197–9202CrossRefPubMedPubMedCentralGoogle Scholar
  20. Rawson PD, Harper FM (2009) Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum. Mar Biol 156:1857–1868CrossRefGoogle Scholar
  21. Reid PC, Johns DG, Edwards M, Starr M, Poulin M, Snoeijs P (2007) A biological consequence of reducing Arctic ice cover: arrival of the Pacific diatom Neodenticula seminae in the North Atlantic for the first time in 800 000 years. Glob Chang Biol 13:1910–1921CrossRefGoogle Scholar
  22. Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400CrossRefPubMedGoogle Scholar
  23. Riginos C, Henzler C (2008) Patterns of mtDNA diversity in North Atlantic populations of the mussel Mytilus edulis. Mar Biol 155:399–412CrossRefGoogle Scholar
  24. Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. I. Breeding and settlement. Oecologia 3:277–316CrossRefPubMedGoogle Scholar
  25. Śmietanka B, Zbawicka M, Sańko T, Wenne R, Burzyński A (2013) Molecular population genetics of male and female mitochondrial genomes in subarctic Mytilus trossulus. Mar Biol 160:1709–1721CrossRefPubMedPubMedCentralGoogle Scholar
  26. Theisen BF (1973) The growth of Mytilus edulis L. (bivalva) from Disko and Thule district, Greenland. Ophelia 12:59–77CrossRefGoogle Scholar
  27. Thyrring J, Rysgaard S, Blicher ME, Sejr MK (2015) Metabolic cold adaptation and aerobic performance of blue mussels (Mytilus edulis) along a temperature gradient into the High Arctic region. Mar Biol 162:235–243CrossRefGoogle Scholar
  28. Vainola R, Strelkov P (2011) Mytilus trossulus in Northern Europe. Mar Biol 158(4):817–833CrossRefPubMedPubMedCentralGoogle Scholar
  29. Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307CrossRefGoogle Scholar
  30. Vermeij GJ, Roopnarine PD (2008) The coming Arctic invasion. Science 321:780–781CrossRefPubMedGoogle Scholar
  31. Versteegh EAA, Blicher ME, Mortensen J, Rysgaard S, Als TD, Wanamaker AD (2012) Oxygen isotope ratios in the shell of Mytilus edulis: archives of glacier meltwater in Greenland? Biogeosciences 9:5231–5241CrossRefGoogle Scholar
  32. Wanamaker AD, Kreutz KJ, Borns HW, Introne DS, Feindel S, Funder S, Rawson PD, Barber BJ (2007) Experimental determination of salinity, temperature, growth, and metabolic effects on shell isotope chemistry of Mytilus edulis collected from Maine and Greenland. Paleoceanography 22:PA2217CrossRefGoogle Scholar
  33. Wenne R, Bach L, Zbawicka M, Strand J, McDonald JH (2016) A first report on coexistence and hybridization of Mytilus trossulus and M. edulis mussels in Greenland. Polar Biol 39:343–355CrossRefGoogle Scholar
  34. Wennerström L, Laikre L, Ryman N, Utter FM, Ab Ghani NI, André C, DeFaveri J, Johansson D, Kautsky L, Merilä J, Mikhailova N, Pereyra R, Sandström A, Teacher AGF, Wenne R, Vasemägi A, Zbawicka M, Johannesson K, Primmer CR (2013) Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management. Biodivers Conserv 22:3045–3065CrossRefGoogle Scholar
  35. Węsławski MJ, Kendall AM, Włodarska-Kowalczuk M, Iken K, Kędra M, Legezynska J, Sejr KM (2011) Climate change effects on Arctic fjord and coastal macrobenthic diversity—observations and predictions. Mar Biodivers 41:71–85CrossRefGoogle Scholar
  36. Wisz MS, Broennimann O, Gronkjaer P, Moller PR, Olsen SM, Swingedouw D, Hedeholm RB, Nielsen EE, Guisan A, Pellissier L (2015) Arctic warming will promote Atlantic-Pacific fish interchange. Nat Clim Chang 5:261–265CrossRefGoogle Scholar
  37. Zbawicka M, Skibinski DOF, Wenne R (2003) Doubly uniparental transmission of mitochondrial DNA length variants in the mussel Mytilus trossulus. Mar Biol 142:455–464CrossRefGoogle Scholar
  38. Zbawicka M, Burzyński A, Skibinski D, Wenne R (2010) Scottish Mytilus trossulus mussels retain ancestral mitochondrial DNA: complete sequences of male and female mtDNA genomes. Gene 456:45–53CrossRefPubMedGoogle Scholar
  39. Zbawicka M, Drywa A, Smietanka B, Wenne R (2012) Identification and validation of novel SNP markers in European populations of marine Mytilus mussels. Mar Biol 159:1347–1362CrossRefGoogle Scholar
  40. Zbawicka M, Sanko T, Strand J, Wenne R (2014) New SNP markers reveal largely concordant clinal variation across the hybrid zone between Mytilus spp. in the Baltic Sea. Aquat Biol 21:25–36Google Scholar
  41. Zbawicka M, Trucco MI, Wenne R. (2018) Single nucleotide polymorphisms in native South American Atlantic coast populations of smooth shelled mussels: hybridization with invasive European Mytilus galloprovincialis. Genetics Selection Evolution 50:5Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Arctic Research Centre, Department of BioscienceAarhus UniversityAarhusDenmark
  2. 2.Department of Genetics and Marine Biotechnology, Institute of OceanologyPolish Academy of SciencesSopotPoland

Personalised recommendations