Abstract
The pelagic snail Limacina helicina Phipps, 1774 is widely distributed in high-latitude seas and is a sensitive bioindicator of ocean acidification. It is known that the response patterns to ocean acidification differ among populations within or among species. Thus, it is important to understand their genetic population structure and identify the cryptic species. L. helicina displays different shell morphotypes, called “formae,” in different regions (North Atlantic, L. helicina forma helicina Phipps, 1774; Northwest Pacific, L. helicina f. acuta Spoel, 1967; Northeast Pacific, L. helicina f. pacifica Dall, 1871; Okhotsk Sea, L. helicina f. ochotensis Shkoldina, 1999: Spoel, 1967, pp. 257, 349). A recent study by Shimizu et al. (Journal of Molluscan Studies 84:30-37, 2018) showed clear genetic differentiation between two formae, L. helicina forma helicina (Svalbard in the Arctic Ocean) and L. helicina f. acuta (station K2 in the western North Pacific) (ΦCT = 0.59282), using partial mitochondrial cytochrome c oxidase subunit I (COI) gene sequences. However, whether other formae of this species are genetically distinct remain unknown. Here we focused on L. helicina f. ochotensis, which inhabits the Sea of Okhotsk, and compared its shell morphology and partial mitochondrial COI gene sequences with another forma, L. helicina f. acuta, which is found in the western North Pacific. We found differences in the shell morphology of L. helicina f. ochotensis collected from the Sea of Okhotsk (off the coast of Monbetsu, Hokkaido, Japan) and L. helicina f. acuta collected from the western North Pacific (station K2). However, molecular analysis of an mtDNA COI region (503 bp) revealed that most individuals collected from Monbetsu (Sea of Okhotsk) were haplotype 1 (75.5%), which is also the major haplotype found in L. helicina f. acuta (western North Pacific). Our results suggest that individuals of L. helicina are frequently dispersed between the Sea of Okhotsk and the western North Pacific by ocean currents. Thus, the two formae, L. helicina f. acuta and L. helicina f. ochotensis, are more likely to be attributable to phenotypic plasticity in response to different environmental parameters, such as temperature and salinity, than to differences in their genetic backgrounds.
References
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge. https://doi.org/10.1093/icb/41.1.134
Bednaršek N, Tarling GA, Bakker DC et al (2012) Description and quantification of pteropod shell dissolution: a sensitive bioindicator of ocean acidification. Glob Chang Biol 18:2378–2388. https://doi.org/10.1111/j.1365-2486.2012.02668.x
Burridge AK, Goetze E, Raes N, Huisman J, Peijnenburg KT (2015) Global biogeography and evolution of Cuvierina pteropods. BMC Evol Biol 15:39. https://doi.org/10.1186/s12862-015-0310-8
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Dall WH (1871) Descriptions of sixty new forms of mollusks from the west coast of North America and the North Pacific Ocean, with notes on others already described. Am J Conchol 7:93–160 https://www.biodiversitylibrary.org/page/15918248
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 Resour 10:564–567
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299 https://pubmed.ncbi.nlm.nih.gov/7881515/
Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59:2378–2398. https://doi.org/10.1111/j.0014-3820.2005.tb00948.x
Hunt B, Strugnell J, Bednarsek N, Linse K, Nelson RJ, Pakhomov E, Seibel B, Steinke D, Würzberg L (2010) Poles apart: the ‘bipolar’ pteropod species Limacina helicina is genetically distinct between the Arctic and Antarctic oceans. PLoS One 5:e9835
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Klingenberg C (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Dev Genes Evol 226(3):113–137. https://doi.org/10.1007/s00427-016-0539-2
Lalli CM, Gilmer RW (1989) Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford University Press, Stanford
Maas AE, Blanco-Bercial L, Lawson GL (2013) Reexamination of the species assignment of Diacavolinia pteropods using DNA barcoding. PLoS One 8:e53889. https://doi.org/10.1371/journal.pone.0053889
Manno C, Bednaršek N, Tarling GA et al (2017) Shelled pteropods in peril: assessing vulnerability in a high CO2 ocean. Earth Sci Rev 169:132–145. https://doi.org/10.1016/j.earscirev.2017.04.005
Mcgowan JA (1963) Geographical variation in Limacina helicina in the North Pacific. In: Speciation in the sea. Harding JP & Tebble N (eds). Syst Ass London 5:109–128
Paranjape MA (1968) The egg mass and veligers of Limacina helicina Phipps. Veliger 10:322–326
Phipps CJ (1774) A voyage towards the North Pole undertaken by His Majesty’s command 1773. Printed by W. Bowyer and J. Nicols, for J. Nourse, London. https://doi.org/10.5962/bhl.title.740
Questel JM, Blanco-Bercial L, Hopcroft RR, Bucklin A (2016) Phylogeography and connectivity of the Pseudocalanus (Copepoda: Calanoida) species complex in the eastern North Pacific and the Pacific Arctic Region. J Plankton Res 38:610–623. https://doi.org/10.1093/plankt/fbw025
Shimizu K, Kimoto K, Noshita K, Wakita M, Fujiki T, Sasaki T (2018) Phylogeography of the pelagic snail Limacina helicina (Gastropoda: Thecosomata) in the subarctic western North Pacific. J Molluscan Stud 84:30–37. https://doi.org/10.1093/mollus/eyx040
Shkoldina LS (1999) On the systematics of the pteropod mollusk Limacina helicina from the Sea of Okhotsk. Russ J Mar Biol 25:330–336
Van Der Spoel S (1967) Euthecosomata: a group with remarkable developmental stages (Gastropoda, Pteropoda). J. Noorduijn en Zoon N. V, Gorinchem ISBN: 978-90-04-07153-7
Sromek L, Lasota R, Wolowicz M (2015) Impact of glaciations on genetic diversity of pelagic mollusks: Antarctic Limacina antarctica and Arctic Limacina helicina. Mar Ecol Prog Ser 525:143–152. https://doi.org/10.3354/meps11237
Yebra L, Bonnet D, Harris RP, Lindeque PK, Peijnenburg KTCA (2011) Barriers in the pelagic: population structuring of Calanus helgolandicus and C. euxinus in European waters. Mar Ecol Prog Ser 428:135–149. https://doi.org/10.3354/meps09056
Acknowledgments
We thank Erena Shima (Ishinomaki Senshu University), Daichi Arima (Hokkaido University), Seiji Katakura and Katsushi Iwamoto (City of Monbetsu), and Katsushi Murai (Garinko & Okhotsk Tower Co., Ltd.) for the collection of Limacina helicina. We also thank two professional editors who are both native speakers of English for editing English in this manuscript.
Funding
This study was funded by the JSPS Grants-in-Aid for Scientific Research (15H06908 and 16H04961).
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.
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All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgments, if applicable.
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All sequences generated by this study have been publicly opened in GenBank (Accession numbers LC377066-LC377118).
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K.S., K.K., K.N., and T.S. conceived and designed research. K.S. and K.K. collected the samples. K.S. generated the genetic data and analyzed them. K.K. generated the 3D data using micro-X-ray CT. K.N. conducted shell morphological analyses. K.S. and K.N. wrote the manuscript. All authors read and approved the manuscript.
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Communicated by C. Chen
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Shimizu, K., Noshita, K., Kimoto, K. et al. Phylogeography and shell morphology of the pelagic snail Limacina helicina in the Okhotsk Sea and western North Pacific. Mar. Biodivers. 51, 22 (2021). https://doi.org/10.1007/s12526-021-01166-z
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DOI: https://doi.org/10.1007/s12526-021-01166-z