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Two cryptic species of the Hediste diversicolor group (Polychaeta, Nereididae) in the Baltic Sea, with mitochondrial signatures of different population histories

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Abstract

A presence of two cryptic biological species of Hediste diversicolor complex polychaetes was corroborated in a geographical survey of some 30 populations from the eastern and southern coasts of the Baltic Sea, with data from four completely diagnostic allozyme characters. Species A was dominant in the northernmost part of the Baltic Hediste range (Bothnian Sea), whereas Species B alone was found in the south (Poland, Germany, Denmark). In the intervening region, comprising the majority of the sites studied in southern Finland and Estonia, the two species were usually found together, with no evidence of recent hybridisation (i.e., no heterozygote genotypes). While mitochondrial DNA also distinguished the two taxa, it was not similarly completely diagnostic, but there were rare cases (ca 5%) of lineage mismatch indicating that some introgression has occurred in the past. Comparison with published data suggests that species A also inhabits the North Sea–NE Atlantic–Mediterranean coasts, and species B is also present in the North Sea and the NW Atlantic (Canada). Within the Baltic, the two species show distinctly different patterns of mtDNA diversity, plausibly related to different colonisation histories. Species A shows a generally high haplotype and nucleotide diversity, whereas in species B we found only four deeply diverged groups of closely related haplotypes. Hypothetically this could indicate a recent expansion of species B from a small number of colonising individuals. Moreover, species B showed marked intraspecific geographical structuring, with co-incident genetic changes along the N Estonian–S Finnish coasts both in mtDNA and an allozyme marker; this pattern suggests a contact between two genetically distinct invasion waves of different origins. In all, species A and B represent good, reproductively isolated and partly sympatric species which require to be recognised in ecological work. A formal taxonomical description is needed, but awaits better, range-wide distributional and ecological characterisation and working out of morphological differences that enable a practical identification.

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References

  • Audzijonytė A, Väinölä R (2005) Diversity and distributions of circumpolar fresh- and brackish-water Mysis (Crustacea: Mysida): descriptions of M. relicta Lovén, 1862, M. salemaai n. sp., M. segerstralei n. sp. and M. diluviana n. sp., based on molecular and morphological characters. Hydrobiologia 544:89–141. doi:10.1007/s10750-004-8337-7

    Article  Google Scholar 

  • Audzijonyte A, Väinölä R (2006) Phylogeographic analyses of a circumarctic coastal and a boreal lacustrine mysid crustacean, and evidence of fast post-glacial mtDNRA rates. Mol Ecol 15:3287–3301. doi:10.1111/j.1365-294X.2006.02998.x

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (2000) Phylogeography. Harvard University Press, Cambridge

    Google Scholar 

  • Bastrop R, Blank M (2006) Multiple invasions—a polychaete genus enters the Baltic Sea. Biol Invasions 8:1195–1200. doi:10.1007/s10530-005-6186-6

    Article  Google Scholar 

  • Bastrop R, Röhner M, Sturmbauer C, Jürss K (1997) Where did Marenzelleria spp. (Polychaeta: Spionidae) in Europe come from? Aquat Ecol 31:119–136. doi:10.1023/A:1009994102526

    Article  Google Scholar 

  • Bastrop R, Jürss K, Sturmbauer C (1998) Cryptic species in a marine polychaete and their independent introduction from North America to Europe. Mol Biol Evol 15:97–103

    Article  CAS  PubMed  Google Scholar 

  • Bernatchez L, Glémet H, Wilson CC, Danzmann RG (1995) Introgression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 52:179–185. doi:10.1139/f95-018

    Article  CAS  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K et al (2006) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. doi:10.1016/j.tree.2006.11.004

    Article  PubMed  Google Scholar 

  • Blank M, Laine AO, Jürss K, Bastrop R (2008) Molecular species identification key based on PCR/RFLP for discrimination of three polychaete sibling species of the genus Marenzelleria, and their current distribution in the Baltic Sea. Helgol Mar Res 62:129–141. doi:10.1007/s10152-007-0081-8

    Article  Google Scholar 

  • Boore J, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17:87–106

    Article  CAS  PubMed  Google Scholar 

  • Breton S, Dufresne F, Desrosiers G, Blier PU (2003) Population structure of two northern hemisphere polychaetes, Neanthes virens and Hediste diversicolor (Nereididae), with different life-history traits. Mar Biol (Berl) 142:707–715

    Article  CAS  Google Scholar 

  • Cristescu MEA, Hebert PDN, Witt JDS, MacIsaac HJ, Grigorovich IA (2001) An invasion history for Cercopagis pengoi based on mitochondrial gene sequences. Limnol Oceanogr 46:224–229

    Article  Google Scholar 

  • Cristescu MEA, Witt JDS, Grigorovich IA, Hebert PDN, MacIsaac HJ (2004) Dispersal of the Ponto-Caspian amphipod Echinogammarus ischnus: invasion waves from the Pleistocene to the present. Heredity 92:197–203. doi:10.1038/sj.hdy.6800395

    Article  CAS  PubMed  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 131:479-491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    Article  CAS  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319. doi:10.1111/j.1096-0031.1994.tb00181.x

    Article  Google Scholar 

  • Folmer O, Black M, Hoen 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

    CAS  PubMed  Google Scholar 

  • Fong PP, Garthwaite RL (1994) Allozyme electrophoretic analysis of the Hediste limnicolaH. diversicolorH. japonica species complex (Polychaeta: Nereididae). Mar Biol (Berl) 118:463–470. doi:10.1007/BF00350303

    Article  CAS  Google Scholar 

  • Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570

    CAS  PubMed  PubMed Central  Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Syst 34:397–423. doi:10.1146/annurev.ecolsys.34.011802.132421

    Article  Google Scholar 

  • Goudet J (1995) Fstat version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Hebert PDN, Ratnasingham S, DeWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci 270(Suppl):S96–S99

    Article  CAS  Google Scholar 

  • Ho SYW, Larson G (2006) Molecular clocks—when times are a changin’. Trends Genet 22:79–83. doi:10.1016/j.tig.2005.11.006

    Article  CAS  PubMed  Google Scholar 

  • Hurst GDD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B Biol Sci 272:1525–1534

    Article  CAS  Google Scholar 

  • Kijewski TK, Zbawicka M, Väinölä R, Wenne R (2006) Introgression and mitochondrial DNA heteroplasmy in the Baltic populations of mussels Mytilus trossulus and M. edulis. Mar Biol (Berl) 149:1371–1385. doi:10.1007/s00227-006-0316-2

    Article  CAS  Google Scholar 

  • Kontula T, Väinölä R (2001) Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol Ecol 10:1983–2002. doi:10.1046/j.1365-294X.2001.01328.x

    Article  CAS  PubMed  Google Scholar 

  • Leppäkoski E, Gollasch S, Gruszka P, Ojaveer H, Olenin S, Panov V (2002) The Baltic—a sea of invaders. Can J Fish Aquat Sci 59:1175–1188. doi:10.1139/f02-089

    Article  Google Scholar 

  • Müller JC, Hidde D, Seitz A (2002) Canal construction destroys the barrier between major European invasion lineages of the zebra mussel. Proc R Soc Lond B Biol Sci 269:1139–1142

    Article  Google Scholar 

  • Murphy RW, Sites JW, Buth DG Jr, Haufler CH (1996) Proteins: isozyme electrophoresis. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn, Sinauer Associates, Sunderland, MA, pp 51–120

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

    Google Scholar 

  • Nikula R, Strelkov P, Väinölä R (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evol Int J Org Evol 61:928–941. doi:10.1111/j.1558-5646.2007.00066.x

    Article  CAS  Google Scholar 

  • Nikula R, Strelkov P, Väinölä R (2008) A broad transition zone between an inner Baltic hybrid swarm and a pure North Sea subspecies of Macoma balthica (Mollusca, Bivalvia). Mol Ecol 17:1505–1522. doi:10.1111/j.1365-294X.2007.03688.x

    Article  CAS  PubMed  Google Scholar 

  • Ozoh PTE (1992) The importance of adult Hediste (Nereis) diversicolor in managing heavy metal pollution in shores and estuaries. Environ Monit Assess 21:165–171. doi:10.1007/BF00399685

    Article  CAS  PubMed  Google Scholar 

  • Röhner M, Bastrop R, Jürss K (1997) Genetic differentiation in Hediste diversicolor (Polychaeta: Nereididae) for the North Sea and the Baltic Sea. Mar Biol (Berl) 130:171–180. doi:10.1007/s002270050236

    Article  Google Scholar 

  • Scaps P (2002) A review of the biology, ecology and potential use of the common ragworm Hediste diversicolor (OF Müller) (Annelida: Polychaeta). Hydrobiologia 470:203–218. doi:10.1023/A:1015681605656

    Article  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorpe JP (1983) Enzyme variation, genetic distance and evolutionary divergence in relation to levels of taxonomic separation. In: Oxford GS, Rollison D (eds) Protein polymorphism: adaptive and taxonomic siginificance. Academic Press, London, pp 131–152

    Google Scholar 

  • Väinölä R (1986) Sibling species and phylogenetic relationships of Mysis relicta (Crustacea: Mysidacea). Ann Zool Fenn 23:207–221

    Google Scholar 

  • Väinölä R (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Mar Biol (Berl) 143:935–946. doi:10.1007/s00227-003-1137-1

    Article  Google Scholar 

  • Väinölä R, Riddoch BJ, Ward RD, Jones RI (1994) Genetic zoogeography of the Mysis relicta species group (Crustacea: Mysidacea) in northern Europe and North America. Can J Fish Aquat Sci 51:1490–1505

    Article  Google Scholar 

  • Varvio SL, Koehn RK, Väinölä R (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Mar Biol (Berl) 98:51–60. doi:10.1007/BF00392658

    Article  Google Scholar 

  • Virgilio M, Abbiati M (2006) Temporal changes in the genetic structure of intertidal populations of Hediste diversicolor (Polychaeta: Nereididae). J Sea Res 56:53–58. doi:10.1016/j.seares.2006.03.008

    Article  CAS  Google Scholar 

  • Virgilio M, Backeljau T, Abbiati M (2006) Mitochondrial DNR and allozyme patterns of Hediste diversicolor (Polychaeta: Nereididae): the importance of small scale genetic structuring. Mar Ecol Prog Ser 326:157–165. doi:10.3354/meps326157

    Article  CAS  Google Scholar 

  • Waters JM, Rowe DL, Apte S, King TM, Wallis GP, Anderson L et al (2007) Geological dates and molecular rates: rapid divergence of rivers and their biotas. Syst Biol 56:271–282. doi:10.1080/10635150701313855

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641

    CAS  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 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank all those who kindly sent us samples or helped in the field, including D. Daunys, M. Daneliya, J. Kotta, R. Nikula and M. Reinikainen. Special thanks to S. Nielsen for help with most of the sampling, even after losing his car to thieves (hence the absence of frozen samples from Latvia). We also thank three anonymous referees for insightful comments. The study has been supported by grants from the Walter and Andrée de Nottbeck Foundation and the University of Helsinki research funds.

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Correspondence to Asta Audzijonyte.

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Communicated by S. Uthicke.

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Audzijonyte, A., Ovcarenko, I., Bastrop, R. et al. Two cryptic species of the Hediste diversicolor group (Polychaeta, Nereididae) in the Baltic Sea, with mitochondrial signatures of different population histories. Mar Biol 155, 599–612 (2008). https://doi.org/10.1007/s00227-008-1055-3

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