Abstract
Despite the ecological importance of copepods Pseudocalanus spp., no genetic analyses have been carried out for these species in the western North Pacific. This study investigated the genetic structures of Pseudocalanus spp. in the Okhotsk Sea using mitochondrial cytochrome c oxidase subunit I (mtCOI) and single nucleotide polymorphism data obtained using multiplexed inter-simple sequence repeat genotyping by sequencing (MIG-seq). Pseudocalanus acuspes was detected based on mtCOI for the first time in the Okhotsk Sea, along with the common species P. minutus and P. newmani in the western North Pacific. The coastal species, P. acuspes and P. newmani, showed unique populations in the Okhotsk Sea, distinct from those in the Bering, Chukchi, Beaufort Seas, and the Atlantic Ocean. However, P. minutus with oceanic distribution patterns showed high gene flow and no clear population in the North Pacific and Pacific Arctic regions. The higher genetic diversity observed in P. newmani compared to P. acuspes and P. minutus was likely due to the wider distribution of P. newmani tolerant to warm waters. A different genetic population structure between the Okhotsk Sea and the Arctic Ocean in P. acuspes was not detected by mtCOI but by MIG-seq analysis. Thus, ecological differences strongly influence the genetic population structures of three Pseudocalanus species in the Okhotsk Sea; these results suggest the need for genome-wide methods to reveal the detailed population structures of marine zooplankton.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aarbakke ONS, Bucklin A, Halsband C, Norrbin F (2011) Discovery of Pseudocalanus moultoni (Frost, 1989) in Northeast Atlantic waters based on mitochondrial COI sequence variation. J Plankton Res 33:1487–1495. https://doi.org/10.1093/plankt/fbr057
Aarbakke ONS, Bucklin A, Halsband C, Norrbin F (2014) Comparative phylogeography and demographic history of five sibling species of Pseudocalanus (Copepoda: Calanoida) in the North Atlantic Ocean. J Exp Mar Biol Ecol 461:479–488. https://doi.org/10.1016/j.jembe.2014.10.006
Abyzova GA, Nikitin MA, Popova OV, Pasternak AF (2018) Genetic population structure of the pelagic mollusk Limacina helicina in the Kara Sea. PeerJ 6:e5709. https://doi.org/10.7717/peerj.5709
Asami H, Sato H, Shimada H, Sawada M, Miyakoshi Y, Ando D, Nagata M (2007) Influence of physical parameters on zooplankton variability during early ocean life of juvenile chum salmon in the coastal waters of eastern Hokkaido, Okhotsk Sea. N Pac Anadr Fish Comm Bull 4:211–221
Bailey J, Durbin EG, Rynearson T (2016) Species composition and abundance of copepods in the morphologically cryptic genus Pseudocalanus in the Bering Sea. Deep-Sea Res II 134:173–180. https://doi.org/10.1016/j.dsr2.2015.04.017
Blanco-Bercial L, Bucklin A (2016) New view of population genetics of zooplankton: RAD-seq analysis reveals population structure of the North Atlantic planktonic copepod Centropages typicus. Mol Ecol 25:1566–1580. https://doi.org/10.1111/mec.13581
Blanco-Bercial L, Álvarez-Marqués F, Bucklin A (2011) Comparative phylogeography and connectivity of sibling species of the marine copepod Clausocalanus (Calanoida). J Exp Mar Biol Ecol 404:108–111. https://doi.org/10.1016/j.jembe.2011.05.011
Blanco-Bercial L, Cornils A, Copley N, Bucklin A (2014) DNA barcoding of marine copepods: assessment of analytical approaches to species identification. PLoS Curr 6:ecurrents.tol.cdf8b74881f87e3b01d56b43791626d2. https://doi.org/10.1371/currents.tol.cdf8b74881f87e3b01d56b43791626d2
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bucklin A, Bentley A, Franzen S (1998) Distribution and relative abundance of Pseudocalanus moultoni and P. newmani (Copepoda: Calanoida) on Georges Bank using molecular identification of sibling species. Mar Biol 132:97–106. https://doi.org/10.1007/s002270050375
Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley HJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343. https://doi.org/10.1007/s00227-002-0943-1
Bucklin A, Peijnenburg KTCA, Kosobokova KN, O’Brien TD, Blanco-Bercial L, Cornils A, Falkenhaug T, Hopcroft RR, Hosia A, Laakmann S, Li C, Martell L, Questel JM, Wall-Palmer D, Wang M, Wiebe PH, Weydmann-Zwolicka A (2021) Toward a global reference database of COI barcodes for marine zooplankton. Mar Biol 168:78. https://doi.org/10.1007/s00227-021-03887-y
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140. https://doi.org/10.1111/mec.12354
Chen G, Hare MP (2011) Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast. Mol Ecol 20:2425–2441. https://doi.org/10.1111/j.1365-294X.2011.05079.x
Chihara M, Murano M (1997) An Illustrated Guide to Marine Plankton in Japan [In Japanese]. Tokai University Press, Tokyo
Corkett CJ, McLaren IA (1979) The biology of Pseudocalanus. Adv Mar Biol 15:1–231. https://doi.org/10.1016/S0065-2881(08)60404-6
Cullingham CI, Miller JM, Peery RM, Dupuis JR, Malenfant RM, Gorrell JC, Janes JK (2020) Confidently identifying the correct K value using the ΔK method: when does K = 2? Mol Ecol 29:862–869. https://doi.org/10.1111/mec.15374
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510. https://doi.org/10.1038/nrg3012
De Wit P, Dupont S, Thor P (2016) Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evol Appl 9:1112–1123. https://doi.org/10.1111/eva.12335
Deagle BE, Faux C, Kawaguchi S, Meyer B, Jarman SN (2015) Antarctic krill population genomics: apparent panmixia, but genome complexity and large population size muddy the water. Mol. Ecol 24:4943–4959. https://doi.org/10.1111/mec.13370
DeHart HM, Blanco-Bercial L, Passacantando M, Questel JM, Bucklin A (2020) Pathways of Pelagic Connectivity: Eukrohnia hamata (Chaetognatha) in the Arctic Ocean. Front Mar Sci 7:396. https://doi.org/10.3389/fmars.2020.00396
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. https://doi.org/10.1007/s12686-011-9548-7
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Ershova EA, Questel JM, Kosobokova K, Hopcroft RR (2017) Population structure and production of four sibling species of Pseudocalanus spp. in the Chukchi Sea. J Plankton Res 39:48–64. https://doi.org/10.1093/plankt/fbw078
Ershova EA, Nyeggen MU, Yurikova DA, Søreide JE (2021) Seasonal dynamics and life histories of three sympatric species of Pseudocalanus in two Svalbard fjords. J Plankton Res 43:209–223. https://doi.org/10.1093/plankt/fbab007
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
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. https://doi.org/10.1111/j.1755-0998.2010.02847.x
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
Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551. https://doi.org/10.1139/z89-077
Hirai J (2020) Insights into reproductive isolation within the pelagic copepod Pleuromamma abdominalis with high genetic diversity using genome-wide SNP data. Mar Biol 167:1. https://doi.org/10.1007/s00227-019-3618-x
Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6:e1000862. https://doi.org/10.1371/journal.pgen.1000862
Holmborn T, Goetze E, Põllupüü M, Põllumäe A (2011) Genetic species identification and low genetic diversity in Pseudocalanus acuspes of the Baltic Sea. J Plankton Res 33:507–515. https://doi.org/10.1093/plankt/fbq113
Hopcroft RR, Kosobokova KN (2010) Distribution and production of Pseudocalanus species in the Chukchi Sea. Deep-Sea Res II 57:49–56. https://doi.org/10.1016/j.dsr2.2009.08.004
Itoh H, Nishioka J, Tsuda A (2014) Community structure of mesozooplankton in the western part of the Sea of Okhotsk in summer. Prog Oceanogr 126:224–232. https://doi.org/10.1016/j.pocean.2014.05.008
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Kitamura M, Nakagawa Y, Nishino Y, Segawa S, Shiomoto A (2018) Comparison of the seasonal variability in abundance of the copepod Pseudocalanus newmani in Lagoon Notoro-Ko and a coastal area of the southwestern Okhotsk Sea. Polar Sic 15:62–74. https://doi.org/10.1016/j.polar.2017.12.004
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
LeDuc RG, Dizon AE, Burdin AM, Blockin SA, George JC, Brownell RL Jr (2005) Genetic analyses (mtDNA and microsatellites) of Okhotsk and Bering/Chukchi/Beaufort Seas populations of bowhead whales. J Cetacean Res Manage 7:107–111
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Nagai S, Yamamoto K, Hata N, Itakura S (2012) Study of DNA extraction methods for use in loop-mediated isothermal amplification detection of single resting cysts in the toxic dinoflagellates Alexandrium tamarense and A. catenella. Mar Genomics 7:51–56. https://doi.org/10.1016/j.margen.2012.03.002
Nagata M, Miyakoshi Y, Ando D, Fujiwara M, Sawada M, Shimada H, Asami H (2007) Influence of coastal seawater temperature on the distribution and growth of juvenile chum salmon, with recommendations for altered release strategies. N Pac Anadr Fish Comm Bull 4:223–235
Nakagawa Y, Ichikawa H, Kitamura M, Nishino Y (2015) Copepod community succession during warm months in Lagoon Notoro-ko, northeastern Hokkaido, Japan. Polar Sci 9:249–257. https://doi.org/10.1016/j.polar.2015.02.001
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 381:129–138. https://doi.org/10.3354/meps07940
Norrbin MF (1991) Gonad maturation as an indication of seasonal cycles for several species of small copepods in the Barents Sea. Polar Res 10:421–432. https://doi.org/10.1111/j.1751-8369.1991.tb00663.x
Nuwer ML, Frost BW, Virginia Armbrust E (2008) Population structure of the planktonic copepod Calanus pacificus in the North Pacific Ocean. Mar Biol 156:107–115. https://doi.org/10.1007/s00227-008-1068-y
Oshima KI, Wakatsuchi M, Fukamachi Y, Mizuta G (2002) Near-surface circulation and tidal currents of the Okhotsk Sea observed with satellite-tracked drifters. J Geophys Res 107(C11):3195. https://doi.org/10.1029/2001JC001005
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Peijnenburg KT, Goetze E (2013) High evolutionary potential of marine zooplankton. Ecol Evol 3:2765–2781. https://doi.org/10.1002/ece3.644
Pinchuk AI, Paul AJ (2000) Zooplankton of the Okhotsk Sea: a review of Russian studies. Alaska Sea Grant College, Fairbanks
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945y
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
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
Samatov AD (2001) Pseudocalanus species (Copepoda: Calanoida) in Avachinskaya Bay, Southeastern Kamchatka. Russ J Mar Biol 27:218–226. https://doi.org/10.1023/A:1011911319002
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
Shimizu K, Noshita K, Kimoto K, Sasaki T (2021) Phylogeography and shell morphology of the pelagic snail Limacina helicina in the Okhotsk Sea and western North Pacific. Mar Biodivers 51:22. https://doi.org/10.1007/s12526-021-01166-z
Smirnova MA, Orlova SY, Mugue NS, Mukhametov IN, Smirnov AA, Orlov AM (2015) Genetic differentiation of Pacific cod Gadus macrocephalus in the Sea of Okhotsk and in the Bering Sea. Dokl Biochem Biophys 465:389–393. https://doi.org/10.1134/S1607672915060113
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Suyama Y, Matsuki Y (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci Rep 5:16963. https://doi.org/10.1038/srep16963
Suyama Y, Hirota SK, Matsuo A, Tsunamoto Y, Mitsuyuki C, Shimura A, Okano K (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecol Res 37:171–181. https://doi.org/10.1111/1440-1703.12270
Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
Unal E, Frost BW, Armbrust V, Kideys AE (2006) Phylogeography of Calanus helgolandicus and the Black Sea copepod Calanus euxinus, with notes on Pseudocalanus elongatus (Copepoda, Calanoida). Deep-Sea Res II 53:1961–1975. https://doi.org/10.1016/j.dsr2.2006.03.017
Weingartner T, Aagaard K, Woodgate R, Danielson S, Sasaki Y, Cavalieri D (2005) Circulation on the north central Chukchi Sea shelf. Deep-Sea Res II 52:3150–3174. https://doi.org/10.1016/j.dsr2.2005.10.015
Wessel P, Smith WHF, Scharroo R, Luis J, Wobbe F (2013) Generic Mapping Tools: improved version released. EOS Trans AGU 94:409–410. https://doi.org/10.1002/2013EO450001
Weydmann A, Przyłucka A, Lubośny M, Walczyńska KS, Serrão EA, Pearson GA, Burzyński A (2018) Postglacial expansion of the Arctic keystone copepod Calanus glacialis. Mar Biodivers 48:1027–1035. https://doi.org/10.1007/s12526-017-0774-4
Acknowledgements
We thank the captains, crews, and all members of Garinko-II and RV Hakuho-maru for assisting with field sampling during the cruises. We thank H. Yoshida for assisting with sampling at the Okhotsk Tower in Okhotsk Sea. We are also grateful to M. Noda for her assistance in performing molecular analyses at the laboratory. We also thank the anonymous reviewers for suggestions on the manuscript.
Funding
This study was supported by grants from the Japan Society for the Promotion of Science (grant number: 20H03057) and Asahi Glass Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
All applicable international, national, and/or institutional guidelines for animal testing, animal 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.
Data availability
The mtCOI sequences obtained in this study are publicly available from GenBank (accession numbers LC705904–LC706198). Raw MIG-seq sequence data are available from the NCBI/EBI/DDBJ Sequence Read Archive (BioProject accession number PRJDB13375).
Author contribution
JH, SK, and NS conceived and designed the study. Sampling was performed by JH and SK. JH conducted the experiments in a laboratory with the assistance of SN. JH analyzed the data. JH wrote the draft of the manuscript; SK and NS contributed to reviewing and editing the manuscript.
Additional information
Communicated by S. Ohtsuka
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 633 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hirai, J., Katakura, S. & Nagai, S. Comparisons of genetic population structures of copepods Pseudocalanus spp. in the Okhotsk Sea: the first record of P. acuspes in coastal waters off Japan. Mar. Biodivers. 53, 12 (2023). https://doi.org/10.1007/s12526-022-01323-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-022-01323-y