Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T17:14:30.553Z Has data issue: false hasContentIssue false

Morphological and genetic variation in the North Atlantic copepod, Centropages typicus

Published online by Cambridge University Press:  26 July 2011

Claudia Castellani*
Affiliation:
Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, The Hoe, Plymouth PL1 2PB, UK
Alistair J. Lindley
Affiliation:
Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, The Hoe, Plymouth PL1 2PB, UK
Marianne Wootton
Affiliation:
Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, The Hoe, Plymouth PL1 2PB, UK
Christopher M. Lee
Affiliation:
University of Edinburgh
Richard R. Kirby
Affiliation:
University of Plymouth, School of Marine Science and Engineering, Drake Circus, Plymouth PL4 8AA, UK
*
Correspondence should be addressed to: Claudia Castellani, Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, The Hoe, Plymouth PL1 2PB, UK email: cxc@sahfos.ac.uk

Abstract

This study describes phenotypic and genotypic variations in the planktonic copepod, Centropages typicus (Copepoda: Calanoida) that indicate differentiation between geographical samples. We found consistent differences in the morphology of the chela of the sexually modified fifth pereiopod (P5) of male C. typicus between samples from the Mediterranean, western North Atlantic and eastern North Atlantic. A 560 base pairs (bp) region of the C. typicus mitochondrial cytochrome c oxidase subunit I (COI) and a 462 bp fragment of the nuclear rDNA internal transcribed spacer (ITS) tandem array were analysed to determine whether these morphological variations reflect population genetic differentiation. Mitochondrial haplotype diversity was found to be high with 100 unique COI haplotypes among 116 individuals. Analysis of mtCOI variation suggested differentiation between the Mediterranean and Atlantic populations but no separation was detected within the Atlantic. Intragenomic variation in the ITS array suggested genetic differentiation between samples from the western North Atlantic and those from the eastern North Atlantic and Mediterranean. Breeding experiments would be required to elucidate the extent of genetic isolation between C. typicus from the different population centres.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barnard, R., Batten, S.D., Beaugrand, G., Buckland, C., Conway, D.V.P., Edwards, M., Finlayson, J., Gregory, L.W., Halliday, N.C., John, A.W.G., Johns, D.G., Johnson, A.D., Jonas, T.D., Lindley, J.A. and Nyman, J. (2004) Continuous Plankton Records: Plankton Atlas of the North Atlantic Ocean (1958–1999). II. Biogeographical charts. Marine Ecology Progress Series CPR Plankton Atlas Supplement, 1175.Google Scholar
Batten, S.D., Clarke, R., Flinkman, J., Hays, G., John, E., John, A.W.G., Jonas, T.D., Lindley, J.A., Stevens, D. and Walne, A. (2003) CPR sampling: the technical background, materials and methods, and issues of consistency and comparability. Progress in Oceanography 58, 193215.CrossRefGoogle Scholar
Beaugrand, G., Lindley, J.A., Helaouet, P. and Bonnet, D. (2007) Macroecological study of 321 Centropages typicus in the North Atlantic Ocean. Progress in Oceanography 72, 259273.CrossRefGoogle Scholar
Brown, D.D., Wensink, P.C. and Jordan, E. (1972) A comparison of the ribosomal DNAs of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. Journal of Molecular Biology 63, 5773.CrossRefGoogle Scholar
Bucklin, A., Astthorsson, O.S., Gislason, A., Allen, L.D., Smolenack, S.B. and Wiebe, P.H. (2000) Population genetic variation of Calanus finmarchicus in Iceland waters: preliminary evidence of genetic differences between Atlantic and Arctic populations. ICES Journal of Marine Science 57, 15921604.CrossRefGoogle Scholar
Bucklin, A. and Kocher, T.D. (1996) Source regions for recruitment of Calanus finmarchicus to Georges Bank: evidence from molecular population genetic analysis of mtDNA. Deep-Sea Research, Part II 43, 16651681.CrossRefGoogle Scholar
Bucklin, A., Lajeunesse, T.C., Curry, E., Wallinga, J. and Garrison, K. (1996a) Molecular diversity of the copepod, Nannocalanus minor: genetic evidence of species and population structure in the North Atlantic Ocean. Journal of Marine Research 54, 285310.CrossRefGoogle Scholar
Bucklin, A., Smolenack, S.B., Bentley, A.M. and Wiebe, P.H. (1997) Gene flow patterns in the euphausiid, Meganyctiphanes norvegica, in the N Atlantic based on mtDNA sequences for cytochrome b and cytochrome oxidase I. Journal of Plankton Research 19, 17631781.CrossRefGoogle Scholar
Bucklin, A., Sundt, R.C. and Dahle, G. (1996b) The population genetics of Calanus finmarchicus in the North Atlantic. Ophelia 44, 2945.CrossRefGoogle Scholar
Bucklin, A. and Wiebe, P.H. (1998) Low mitochondrial diversity and small effective population sizes of the copepods Calanus finmarchicus and Nannocalanus minor: possible impact of climatic variation during recent glaciation. Journal of Heredity 89, 383392.CrossRefGoogle ScholarPubMed
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual/tutorial. Plymouth: PRIMER-E, 190 pp.Google Scholar
Ehrlich, P.R. and Raven, P.H. (1969) Differentiation of populations. Science 165, 12281232.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P.E. and Quattro, M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Fleminger, A. and Hulsemann, K. (1987) Geographical variation in Calanus helgolandicus s.l. (Copepoda, Calanoida) and evidence of recent speciation of the Black Sea population. Biological Oceanography 5, 4381.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan taxa. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Goetze, E. (2003) Cryptic species on the high seas: global phylogenetics of the copepod family Eucalanidae. Proceedings of the Royal Society B 270, 23212331.CrossRefGoogle ScholarPubMed
Goetze, E. (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59, 23782398.Google ScholarPubMed
Goetze, E. (2008) Heterospecific mating and partial prezygotic reproductive isolation in the planktonic marine copepods Centropages typicus and Centropages hamatus. Limnology and Oceanography 53, 433445.CrossRefGoogle Scholar
Hardy, A.C. (1958) The open sea: its natural history. Part 1. The world of plankton. London: Collins, 335 pp.Google Scholar
Harris, D.J. and Crandall, K.A. (2000) Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Molecular Biology and Evolution 17, 284291.CrossRefGoogle ScholarPubMed
Haury, L.R., McGowan, J.S. and Wiebe, P. (1978) Patterns and processes in the time–space scales of plankton distributions. In Steele, J.H. (ed.) Spatial pattern in plankton communities. New York: Plenum Press, pp. 277327.CrossRefGoogle Scholar
Kirby, R.R., Lindley, J.A. and Batten, S.D. (2007) Spatial heterogeneity and genetic variation in the copepod Neocalanus cristatus along two transects in the North Pacific sampled by the Continuous Plankton Recorder. Journal of Plankton Research 29, 97106.CrossRefGoogle Scholar
Knowlton, N. (1993) Sibling species in the sea. Annual Review of Ecology and Systematics 24, 189216.CrossRefGoogle Scholar
Lee, C.M. (1971) Population structures of the planktonic copepods Centropages typicus and Temora longicornis in the North Atlantic area and functional significance of the reproductive structures of the Centropagidae. PhD thesis. University of Edinburgh, 221 pp.Google Scholar
Lindley, J.A. and Reid, P.C. (2002) Variations in the abundance of Centropages typicus and Calanus helgolandicus in the North Sea: deviations from close relationships with temperature. Marine Biology 141, 153165.Google Scholar
Mauchline, J. (1998) The biology of calanoid copepods. San Diego, CA: Academic Press.Google Scholar
Mazzocchi, M.G., Christou, E.D., Capua, I.D., de Puelles, M.F., Fonda-Umani, S., Molinero, J.C., Nival, P. and Siokou-Frangou, I. (2007) Temporal variability of Centropages typicus in the Mediterranean Sea over seasonal-to-decadal scales. Progress in Oceanography 72, 214232.CrossRefGoogle Scholar
McQuinn, I.H. (1997) Metapopulations and the Atlantic herring. Reviews in Fish Biology and Fisheries 7, 297329.CrossRefGoogle Scholar
Nei, M. (1972) Genetic distance between populations. American Naturalist 106, 283292.CrossRefGoogle Scholar
Nei, M. (1987) Molecular evolutionary genetics. New York: Columbia University Press, 512 pp.CrossRefGoogle Scholar
Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25, 547572.CrossRefGoogle Scholar
Papadopoulus, L.N., Peijnenburg, K.T.C.A. and Luttikhuizen, P.C. (2005) Phylogeography of the calanoid copepods Calanus helgolandicus and Calanus euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. Marine Biology 147, 13531365.CrossRefGoogle Scholar
Patarnello, T., Volckaert, F.A.M.J. and Castillo, R. (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology 16, 44264444.CrossRefGoogle ScholarPubMed
Peakall, R. and Smouse, P.E. (2005) GenAlEx 6: Genetic Analysis in Excel. Population genetic software for teaching and research. Canberra: The Australian National University.Google Scholar
Provan, J., Beatty, G.E., Keating, S.L., Maggs, C.A. and Savidge, G. (2009) High dispersal potential has maintained long-term population stability in the North Atlantic copepod Calanus finmarchicus. Proceedings of the Royal Society B 276, 301307.CrossRefGoogle ScholarPubMed
Razouls, C. (1973) Variations annuelles quantitatives de deux espèces dominantes de copèpodes planctoniques Centropages typicus et Temora stylifera de la région de Baynuls: cycles biologiques et estimations de la production. Cahiers de Biologie Marine 14, 361390.Google Scholar
Staton, J.L., Wickliffe, L.C., Garlitska, L., Villanueva, S.M. and Coull, B.C. (2005) Genetic isolation discovered among previously described sympatric morphs of a meiobenthic copepod. Journal of Crustacean Biology 25, 551557.CrossRefGoogle Scholar
White, T.J., Bruns, T., Lee, S. and Taylor, J.W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, N., Gelfand, D., Sninsky, J and White, T. (eds) PCR—protocols and applications—a laboratory manual. New York: Academic Press, Inc., pp. 315322.Google Scholar
Wright, S. (1931) Evolution in Mendelian populations. Genetics 16, 97159.CrossRefGoogle ScholarPubMed
Zane, L., Ostellari, L., Maccatrozzo, L., Bargelloni, L., Cuzin-Roudy, J., Buchholz, F. and Patarnello, T. (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica, Euphausiacea), from the North East Atlantic and the Mediterranean Sea. Marine Biology 136, 191199.CrossRefGoogle Scholar