Skip to main content
SpringerLink
Log in

Present-day genetic composition suggests contrasting demographic histories of two dominant chaetognaths of the North-East Atlantic, Sagitta elegans and S. setosa

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Sagitta elegans and S. setosa are the two dominant chaetognaths in the North-East (NE) Atlantic. They are closely related and have a similar ecology and life history, but differ in distributional ranges. Sagitta setosa is a typical neritic species occurring exclusively above shelf regions, whereas S. elegans is a more oceanic species with a widespread distribution. We hypothesised that neritic species, because of smaller and more fragmented populations, would have been more vulnerable to population bottlenecks resulting from range contractions during Pleistocene glaciations than oceanic species. To test this hypothesis we compared mitochondrial Cytochrome Oxidase II DNA sequences of S. elegans and S. setosa from sampling locations across the NE Atlantic. Both species displayed very high levels of genetic diversity with unique haplotypes for every sequenced individual and an approximately three times higher level of nucleotide diversity in S. elegans (0.061) compared to S. setosa (0.021). Sagitta setosa mitochondrial DNA (mtDNA) haplotypes produced a star-like phylogeny and a uni-modal mismatch distribution indicative of a bottleneck followed by population expansion. In contrast, S. elegans had a deeper mtDNA phylogeny and a multi-modal mismatch distribution as would be expected from a more stable population. Neutrality tests indicated that assumptions of the standard neutral model were violated for both species and results from the McDonald-Kreitman test suggested that selection played a role in the evolution of their mitochondrial DNA. Congruent with these results, both species had much smaller effective population sizes estimated from genetic data when compared to census population sizes estimated from abundance data, with a factor of ~108–109 difference. Assuming that selective effects are comparable for the two species, we conclude that the difference in genetic signature can only be explained by contrasting demographic histories. Our data are consistent with the hypothesis that in the NE Atlantic, the neritic S. setosa has been more severely affected by population bottlenecks resulting from Pleistocene range shifts than the more oceanic S. elegans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvariño A (1965) Chaetognaths. Oceanogr Mar Biol Ann Rev 3:115–194

    Google Scholar 

  • Andersen BG, Borns HW Jr (1994) The ice age world. Scandinavian Univ Press, Oslo

    Google Scholar 

  • Angel MV (1979) Zoogeography of the Atlantic Ocean. In: Van der Spoel S, Pierrot-Bults AC (eds) Zoogeography and diversity of plankton. Bunge, Utrecht, pp 168–190

    Google Scholar 

  • Angel MV (1993) Biodiversity of the pelagic ocean. Cons Biol 7:760–772

    Article  Google Scholar 

  • Arnaud S, Bonhomme F, Borsa P (1999) Mitochondrial DNA analysis of the genetic relationships among populations of scad mackerel (Decapterus macarellus,D. macrosoma, and D. russelli) in South-East Asia. Mar Biol 135:699–707

    Article  CAS  Google Scholar 

  • Avise JC, Ball RM, Arnold J (1988) Current versus historical population sizes in vertebrate species with high gene flow: a comparison based on mitochondrial DNA lineages and inbreeding theory for neutral mutations. Molec Biol Evol 5:331–344

    PubMed  CAS  Google Scholar 

  • Avise JC, Bowen BW, Lamb T (1989) DNA fingerprints from hypervariable mitochondrial genotypes. Molec Biol Evol 6:258–269

    PubMed  CAS  Google Scholar 

  • Avise JC (2000) Phylogeography. The history and formation of species. Harvard Univ Press, Cambridge

    Google Scholar 

  • Bainbridge V (1963) Continuous plankton records: Contribution towards a plankton atlas of the North Atlantic and the North Sea. VII: Chaetognatha. Hull Bull Mar Ecol 6:40–51

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Molec Ecol 13:729–744

    Article  Google Scholar 

  • Bensasson D, Zhang DX, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaces witnesses. Trends Ecol Evol 16:314–321

    Article  PubMed  Google Scholar 

  • Bieri R (1991) Systematics of the Chaetognatha. In: Bone Q, Kapp H, Pierrot-Bults AC (eds) The biology of Chaetognaths. Oxford press, Oxford, pp 122–136

    Google Scholar 

  • Bone Q, Kapp H, Pierrot-Bults AC (1991) Introduction and relationships of the group. In: Bone Q, Kapp H, Pierrot-Bults AC (eds) The biology of Chaetognaths. Oxford press, Oxford, pp 1–4

    Google Scholar 

  • Borsa P, Blanquer A, Berrebi P (1997) Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Mar Biol 129:233–246

    Article  CAS  Google Scholar 

  • Brookfield JFY, Sharp PM (1994) Neutralism and selectionism face up to DNA data. Trends Genet 10:109–111

    Article  PubMed  CAS  Google Scholar 

  • Bucklin A, Smolenack SB, Bentley AM, Wiebe PH (1997) Gene flow patterns of the euphausiid, Meganyctiphanes norvegica, in the NW Atlantic based on mtDNA sequences for cytochrome b and cytochrome oxidase I. J Plankt Res 19:1763–1781

    Article  CAS  Google Scholar 

  • Bucklin A, Wiebe PH (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. J Hered 89:383–392

    Article  PubMed  CAS  Google Scholar 

  • Bucklin A, Kaartvedt S, Guarnieri M, Goswami U (2000). Population genetics of drifting (Calanus spp.) and resident (Acartia clausi) plankton in Norwegian fjords. J Plankt Res 22:1237–1251

    Article  CAS  Google Scholar 

  • Choe N, Deibel D (2000) Seasonal vertical distribution and population dynamics of the chaetognath Parasagitta elegans in the water column and hyperbenthic zone of Conception Bay, Newfoundland. Mar Biol 137:847–856

    Article  Google Scholar 

  • CLIMAP Project members (1976) The surface of the ice-age earth. Science 191:1131–1137

    Article  Google Scholar 

  • Conway DVP, Williams R (1986) Seasonal population structure, vertical distribution and migration of the chaetognath Sagitta elegans in the Celtic Sea. Mar Biol 93:377–387

    Article  Google Scholar 

  • Dallot S (1968) Observations préliminaires sur la reproduction en élevage du Chaetognathe planctonique Sagitta setosa Müller. Rapp Comm int Mer Médit 19:521–523

    Google Scholar 

  • Donnelly P, Tavaré S (1995) Coalescents and genealogical structure under neutrality. Annu Rev Gen 29:401–421

    Article  CAS  Google Scholar 

  • Dudgeon CL, Gust N, Blair D (2000) No apparent genetic basis to demographic differences in scarid fishes across continental shelf of the Great Barrier Reef. Mar Biol 137:1059–1066

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:497–491

    Google Scholar 

  • Fager EW and McGowan JA (1963) Zooplankton species groups in the North Pacific. Science 140:453–460

    Article  PubMed  Google Scholar 

  • Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583

    PubMed  CAS  Google Scholar 

  • Feigenbaum D (1991) Food and feeding behaviour. In: Bone Q, Kapp H, Pierrot-Bults AC (eds) The biology of Chaetognaths. Oxford press, Oxford, pp 45–54

    Google Scholar 

  • Fraser JH (1952) The Chaetognatha and other zooplankton of the Scottish area and their value as biological indicators of hydrographic conditions. Mar Res Scotl 2:5–52

    Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont A (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134

    Google Scholar 

  • Helfenbein KG, Fourcade HM, Vanjani RG, Boore JL (2004) The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes. Proc Natl Acad USA 101:10639–10643

    Article  CAS  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • 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. Molec Ecol 11:1165–1176

    Article  CAS  Google Scholar 

  • Hoarau G, Piquet AMT, van der Veer HW, Rijnsdorp AD, Stam W, Olsen JL (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190

    Article  CAS  Google Scholar 

  • Holland PWH (1993) Cloning genes using the polymerase chain reaction. In: Stern CD, Holland PWH (eds) Developmental biology: a practical approach. Oxford University Press, Oxford, pp 243–255

    Google Scholar 

  • Jakobsen T (1971) On the biology of Sagitta elegans Verrill and Sagitta setosa J. Müller in Inner Oslofjord. Norw J Zool 19:201–225

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HM (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, London

    Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • McIntyre A, Kipp NG, Bé AWH, Cowley T, Kellogg T, Gardner JV, Prell W, Ruddiman WF (1976) Glacial North Atlantic 18,000 years ago: a CLIMAP reconstruction. In: Cline RM, Hayes JD (eds) Geolog Soc Am Mem 145, pp 43–74

  • Meek A (1928) On Sagitta elegans and Sagitta setosa from the Northumbrian Plankton, with a note on a trematode parasite. Proc Zool Soc Lond 743–776

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

    Google Scholar 

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

    Article  Google Scholar 

  • Øresland V (1983) Abundance, breeding and temporal size distribution of the chaetognath Sagita setosa in the Kattegat. J Plankt Res 5:425–439

    Article  Google Scholar 

  • Øresland V (1986) Temporal distribution of size and maturity stages of the chaetognath Sagitta setosa in the western English Channel. Mar Ecol Prog Ser 29:55–60

    Article  Google Scholar 

  • Øresland V (1987) Feeding of the chaetognaths Sagitta elegans and S. setosa at different seasons in Gullmarsfjorden, Sweden. Mar Ecol Prog Ser 39:69–79

    Article  Google Scholar 

  • Papadopoulos LP, Peijnenburg KTCA, Luttikhuizen PC (2005) Marine Biology. Phylogeography of the calanoid copepods Calanus helgolandicus and C. euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. DOI 10.1007/s00227-005-0038-x

  • Pearre S (1991) Growth and reproduction. In: Bone Q, Kapp H, Pierrot-Bults AC (eds) The biology of Chaetognaths. Oxford press, Oxford, pp 61–75

    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

    PubMed  Google Scholar 

  • Pierrot-Bults AC, Nair VR (1991) Distribution patterns in Chaetognatha. In: Bone Q, Kapp H, Pierrot-Bults AC (eds) The biology of Chaetognaths. Oxford press, Oxford, pp 86–116

    Google Scholar 

  • Pierrot-Bults AC, van der Spoel S (2003). Macrozooplankton diversity: how much do we really know? Zool Verh Leiden 345:297–312

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:917–818

    Article  Google Scholar 

  • Ramos-Onsins S, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molec Biol Evol 19:2092–2100

    PubMed  CAS  Google Scholar 

  • Rodríguez F, Oliver JF, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Russell FS (1932a) On the biology of Sagitta. The breeding and growth of Sagitta elegans Verrill in the Plymouth area, 1930–31. J Mar Biol Assoc UK 18:131–146

    Google Scholar 

  • Russell FS (1932b) On the Biology of Sagitta. II. The breeding and growth of Sagitta setosa J. Müller in the Plymouth area, 1930–31, with a comparison with that of S. elegans Verrill. J Mar Biol Assoc UK 18:147–160

    Article  Google Scholar 

  • Russell FS (1939) Hydrographical and biological conditions in the North Sea as indicated by plankton organisms. J Cons perm Int Explor Mer 14:171–192

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molec Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

  • Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Molec Ecol 8:407–417

    Article  CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved PCR primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Skibinski DOF (2000) DNA tests of neutral theory: applications in marine genetics. Hydrobiologia 420:137–152

    Article  CAS  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP*, phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Assoc, Sunderland

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  CAS  Google Scholar 

  • Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  Google Scholar 

  • Telford MJ, Holland PWH (1997) Evolution of 28S ribosomal DNA in chaetognaths: duplicate genes and molecular phylogeny. J Molec Evol 44:135–144

    Article  PubMed  CAS  Google Scholar 

  • Thuesen EVK, Numachi K, Nemoto T (1993) Genetic variation in the planktonic chaetognaths Parasagitta elegans and Eukrohnia hamata. Mar Ecol Prog Ser 101:243–251

    Article  Google Scholar 

  • Tokioka T (1979) Neritic and oceanic plankton. In: Van der Spoel S, Pierrot-Bults AC (eds) Zoogeography and diversity of plankton. Bunge, Utrecht, pp 126–143

    Google Scholar 

  • Van der Spoel S, Heyman RP (1983) A comparative atlas of zooplankton. Biological patterns in the oceans. Bunge, Utrecht

    Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    Article  PubMed  CAS  Google Scholar 

  • Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics 146:427–441

    PubMed  CAS  Google Scholar 

  • Whittam TS, Nei M (1991) Neutral mutation hypothesis test. Nature 354:115–116

    Article  Google Scholar 

  • Wimpenny RS (1936) The distribution, breeding and feeding of some important plankton organisms of the South-West North Sea in 1934. I. Calanus finmarchius (Gunn), Sagitta setosa (J. Müller) and S. elegans (Verrill). Fish invest Lond 15:1–53

    Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

  • Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Battaglia B Patarnello T (1998) Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations. Proc Roy Soc Lond Ser B 265:2387–2391

    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: Euhausiacea) from the North East Atlantic and the Mediterranean Sea. Mar Biol 136:191–199

    Article  Google Scholar 

Download references

Acknowledgements

We thank all crew of the research vessel Pelagia, R. ter Hofstede, and J.-H Schotveld for their help in taking plankton samples and C. ten Hallers-Tjabes for inviting KP, and H. van Aken for inviting KP and EH aboard their research cruises. H. van Aken is also thanked for his calculations of the areas and volumes of the distributions of the two chaetognaths. W. van Ginkel, P. Kuperus, and B. Voetdijk are acknowledged for laboratory assistance and J. van Arkel for his help with figures. We thank G. Lecaillon, P. Meirmans, A. Pierrot-Bults, and A. Southward for discussion. Comments of J. Breeuwer, M. Egas, M. Genner, P. Luttikhuizen, and S. Menken improved the manuscript. This research was funded by the Netherlands Organisation for Scientific Research (NWO) as part of the priority program ‘Sustainable use and conservation of marine living resources’ project number 885.100.02. Research was carried out in accordance with all laws and regulations of the Netherlands.

Author information

Authors and Affiliations

  1. Institute for Biodiversity and Ecosystem Dynamics, Faculty of Science, Universiteit van Amsterdam, P.O. Box 94062, 1090 GB,  , Amsterdam, The Netherlands

    K. T. C. A. Peijnenburg, E. K. van Haastrecht & C. Fauvelot

Authors
  1. K. T. C. A. Peijnenburg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. K. van Haastrecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Fauvelot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. T. C. A. Peijnenburg.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peijnenburg, K.T.C.A., van Haastrecht, E.K. & Fauvelot, C. Present-day genetic composition suggests contrasting demographic histories of two dominant chaetognaths of the North-East Atlantic, Sagitta elegans and S. setosa . Marine Biology 147, 1279–1289 (2005). https://doi.org/10.1007/s00227-005-0041-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0041-2

Keywords

Search

Navigation