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Population structure of the planktonic copepod Calanus pacificus in the North Pacific Ocean

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Abstract

The pelagic copepod Calanus pacificus ranges nearly continuously across temperate-boreal regions of the North Pacific Ocean and is currently divided into three subspecies—C. pacificus oceanicus, C. pacificus californicus, C. pacificus pacificus—based on subtle morphological differences and geographic location. The relation between geography and genetic differentiation was examined for 398 C. pacificus individuals sampled from six widely distributed locations across the North Pacific, including an open ocean site and coastal sites on both sides of the North Pacific basin. For each individual copepod, the DNA sequence was determined for a 421-bp region of the mitochondrial coxI gene (mtCOI). A total of sixty-three different mtCOI sequences, or haplotypes, were detected, with a sequence divergence between haplotypes of 0.2–3.1%. The number and distribution of haplotypes varied with sampling location; 12 haplotypes were distributed across multiple sampling locations, and 51 occurred at only one location. Five genetically distinct populations were detected based on F ST values. Haplotype minimum spanning networks, nucleotide divergence and F ST values indicated that individuals from coastal sites in the North Pacific Ocean were more closely related to each other than to individuals from the open ocean site at Station P. These results provide genetic support for the designation of two subspecies—a coastal subspecies that consists of what is currently referred to as C. p. pacificus and C. p. californicus and an open ocean subspecies C. p. oceanicus. This work also indicates that planktonic copepods with potentially high dispersal capacity can develop genetically structured populations in the absence of obvious geographic barriers between proximate locales within an ocean basin.

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References

  • Adamowicz SJ, Menu-Marque S, Hebert PD, Purvis A (2007) Molecular systematics and patterns of morphological evolution in Centropagidae (Copepoda:Calanoida) of Argentina. Biol J Linn Soc Lond 90:279–292. doi:https://doi.org/10.1111/j.1095-8312.2007.00723.x

    Article  Google Scholar 

  • Alldredge AL, Robinson BH, Fleminger A, Torres JJ, King JM, Hamner WM (1984) Direct sampling and in situ observation of a persistent copepod aggregation in the mesopelagic zone of the Santa Barbara Basin. Mar Biol (Berl) 80(1):75–81. doi:https://doi.org/10.1007/BF00393130

    Article  Google Scholar 

  • Ayukai T, Nishizawa S (1986) Defecation rate as a possible measure of ingestion rate of Calanus pacificus pacificus (Copepoda: Calanoida). Bull Plankton Soc Japan 33:3–10

    Google Scholar 

  • Bradford JM (1988) Review of the taxonomy of the Calanidae (Copepoda) and the limits to the genus Calanus. Hydrobiologia 167/168:73–81. doi:https://doi.org/10.1007/BF00026295

    Article  Google Scholar 

  • Brodsky KA (1965) The taxonomy of marine plankton organisms and oceanography. Oceanology (Mosc) 5(4):1–12

    Google Scholar 

  • Bucklin A (2000) Methods for population genetic analysis of zooplankton. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) Zooplankton methodology manual. Academic Press, San Diego, pp 533–570

    Chapter  Google Scholar 

  • Bucklin A, Lajeunesse TC (1994) Molecular genetic variation of Calanus pacificus Copepoda: Calanoida): preliminary evaluation of genetic structure and subspecific differentiation based on mtDNA sequences. Rep CCOFI 35:45–51

    Google Scholar 

  • Bucklin A, Frost BW, Kocher TD (1995) Molecular systematics in six Calanus and three Metridia species (Calanoida: Copepoda). Mar Biol (Berl) 121:655–664. doi:https://doi.org/10.1007/BF00349301

    Article  CAS  Google Scholar 

  • Bucklin A, LaJeunesse TC, Curry E, Wallinga J, Garrison K (1996) Molecular diversity of the copepod, Nannocalanus minor: genetic evidence of species and population structure in the North Atlantic Ocean. J Mar Res 54(2):285–310. doi:https://doi.org/10.1357/0022240963213385

    Article  Google Scholar 

  • Bucklin A, Guarnieri M, McGillicuddy D, Hill RS (2000a) Spring-summer evolution of Pseudocalanus spp. abundance on Georges Bank based on molecular discrimination of P. moultoni and P. newmani. Deep Sea Res Part II Top Stud Oceanogr 48:589–608. doi:https://doi.org/10.1016/S0967-0645(00)00128-4

    Article  Google Scholar 

  • Bucklin A, Astthorsson OS, Gislason A, Allen LD, Smolenack SB, Wiebe PH (2000b) Population genetic variation of Calanus finmarchicus in Icelandic waters: preliminary evidence of genetic differences between Atlantic and Arctic populations. J Mar Sci 57(6):1592–1604

    Google Scholar 

  • Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley ND (2003) Molecular systematic phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol (Berl) 142:333–343

    Article  CAS  Google Scholar 

  • Conover RJ (1988) Comparitive life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia 167:127–142

    Article  Google Scholar 

  • Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahms HU (1995) Dormancy in the Copepoda—an overview. Hydrobiologia 306:199–211. doi:https://doi.org/10.1007/BF00017691

    Article  Google Scholar 

  • DeDecker AHB, Kaczmaruk BZ, Marska G (1991) A new species of Calanus (Copepoda, Calanoida) from South African waters. Ann S Afr Mus 101(3):27–44

    Google Scholar 

  • Duda TF Jr, Palumbi SR (1999) Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations. Mar Biol (Berl) 134:705–710. doi:https://doi.org/10.1007/s002270050586

    Article  Google Scholar 

  • Excoffier L, Smouse P (1994) Using allele frequencies and geographic subdivision to reconstruct genealogies within a species. Genetics 136:343–359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fleminger A (1985) Dimorphism and possible sex change in copepods of the family Calanidae. Mar Biol 88(3):273–294

    Article  Google Scholar 

  • Fleminger A, Hulsemann K (1977) Geographical range and taxonomic divergence in North Atlantic Calanus (Calanus helgolandicus, Calanus finmarchicus and Calanus glacialis). Mar Biol 40(3):233–248

    Article  Google Scholar 

  • Frost BW (1988) Variability and the possible adaptive significance of diel vertical migration in Calanus pacificus, a planktonic marine copepod. Bull Mar Sci 43(3):675–694

    Google Scholar 

  • Goetze E (2003) Cryptic speciation on the high seas; global phylogenetics of the copepod family Eucalanidae. Proc R Soc Lond B 270:2321–2331

    Article  Google Scholar 

  • Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59(11):2378–2398

    CAS  Google Scholar 

  • Goetze E, Bradford-Grieve J (2005) Genetic and morphological description of Eucalanus spinifer T. Scott, 1894 (Calanoida: Eucalanidae), a circumglobal sister species of the coepod E. hyalinus s.s. (Claus, 1866). Prog Oceanogr 65:55–87

    Article  Google Scholar 

  • Grishanin AK, Rasch EM, Dodson SI, Wyngaard GA (2006) Genetic architecture of the cryptic species complex of Acanthocyclops vernalis (Crustacea: Copepoda). II. Crossbreeding experiments, cytogenetics, and a model of chromosomal evolution. Evolution 60(2):247–256

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hill RS, Allen LD, Bucklin A (2001) Multiplexed species-specific PCR protocol to discriminate four N. Atlantic Calanus species, with an mtCOI gene tree for ten Calanus species. Mar Biol 139(2):279–287

    Article  CAS  Google Scholar 

  • Hulsemann K (1991) Calanus euxinus, new name, a replacement name for Calanus ponticus Karavaev, 1894 (Copepoda, Calanoida). Proc Biol Soc Wash 104(3):620–621

    Google Scholar 

  • Hulsemann K (1994) Calanus sinicus Brodsky and C. jashnovi, nom. nov. (Copepoda: Calanoida) of the North-west Pacific Ocean: A comparison, with notes on the integumental pore pattern in Calanus s. str. Invertebr. Taxon 8(6):1461–1482

    Article  Google Scholar 

  • Johnson CL (2007) Retention of dormant coepods in deep basins of the Southern California Bight. Mar Ecol Prog Ser 336:203–210

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Lee CE, Frost BW (2002) Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480:111–128

    Article  CAS  Google Scholar 

  • McLean JE, Hay DE, Taylor EB (1999) Marine population structure in an anadromous fish: life history influences patterns of mitochondrial DNA variation in the eulachon, Thaleichthys pacificus. Mol Ecol 8:S143–S158

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Norris RD (2000) Pelagic species diversity, biogeography, and evolution. Paleobiology 26S:236–258

    Article  Google Scholar 

  • Ohman MD (1988) Sources of variability in measurements of copepod lipids and gut fluorescence in the California Current coastal zone. Mar Ecol Prog Ser 42:143–153

    Article  CAS  Google Scholar 

  • Ohman MD, Drits AV, Clarke ME, Plourde S (1998) Differential dormancy of co occurring copepods. Deep Sea Res Part II Top Stud Oceanogr 45:1709–1740

    Article  Google Scholar 

  • Osgood KE, Checkley DM Jr (1997a) Observations of a deep aggregation of Calanus pacificus in the Santa Barbara Basin. Limnol Oceanogr 42:997–1001

    Article  Google Scholar 

  • Osgood KE, Checkley DM Jr (1997b) Seasonal variations in a deep aggregation of Calanus pacificus in the Santa Barbara Basin. Mar Ecol Prog Ser 148:59–69

    Article  Google Scholar 

  • Osgood KE, Frost BW (1994) Comparative life histories of three species of planktonic calanoid copepods in Dabob Bay, Washington. Mar Biol 118:627–636

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517

    Article  Google Scholar 

  • Papetti C, Zane L, Bortolotto E, Bucklin A, Patarnello T (2005) Genetic differentiation and local temporal stability of population structure in the euphausiid Meganyctiphanes norvegica. Mar Ecol Prog Ser 289:225–235

    Article  CAS  Google Scholar 

  • Peijnenburg KTCA, Breeuwer JAJ, Pierrot-Bults AC, Menken SBJ (2004) Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European seas. Evolution 58:1472–1487

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Bio and Evol 9:552–569

    CAS  Google Scholar 

  • Runge JA (1985) Relationship of egg production of Calanus pacificus to seasonal changes in phytoplankton availability in Puget Sound, Washington. Limnol Oceanogr 30(2):382–396

    Article  Google Scholar 

  • Schneider S, Kueffer J, Roessli D, Excoffier L (1997) Arlequin. V11. A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

    Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson J (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  Google Scholar 

  • Ury HK (1976) A comparison of four procedures for multiple comparisons among means (pairwise contrasts) for arbitrary sample sizes. Technometrics 18(1):89–97

    Article  Google Scholar 

  • Uye S (1988) Temperature dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia 167/168:285–293

    Article  Google Scholar 

  • Van der Spoel S (1994) The basis for boundaries in pelagic biogeography. Prog Oceanogr 34:121–133

    Article  Google Scholar 

  • Welschmeyer NA, Lorenzen CJ (1985) Role of herbivory in controlling phytoplankton abundance–annual pigment budget for a temperate marine fjord. Mar Biol 90(1):75–86

    Article  CAS  Google Scholar 

  • Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Cuzin-Roudy J, Buchholz F, Patarnello T (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica: Euphausiacea) from the North east Atlantic and the Mediterranean Sea. Mar Biol 136:191–199

    Article  Google Scholar 

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Acknowledgments

We thank B. Peterson, M. Galbraith, R. Goldblatt, E. Goetze, K. Kuma, J. J. Pierson, and A. Yamaguchi for collecting plankton samples used in the present study. Many thanks to A. Bucklin for scientific advice and encouragement. This manuscript has benefitted from the comments of two anonymous reviewers.

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  1. School of Oceanography, University of Washington, Seattle, WA, 98195, USA

    Mikelle L. Nuwer, Bruce W. Frost & E. Virginia Armbrust

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  1. Mikelle L. Nuwer
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  2. Bruce W. Frost
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  3. E. Virginia Armbrust
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Correspondence to Mikelle L. Nuwer.

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Communicated by M.I. Taylor.

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Nuwer, M.L., Frost, B.W. & Virginia Armbrust, E. Population structure of the planktonic copepod Calanus pacificus in the North Pacific Ocean. Mar Biol 156, 107–115 (2008). https://doi.org/10.1007/s00227-008-1068-y

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