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BMC Evolutionary Biology Biomed Central View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by OceanRep BMC Evolutionary Biology BioMed Central Research article Open Access Mitochondrial sequence data expose the putative cosmopolitan polychaete Scoloplos armiger (Annelida, Orbiniidae) as a species complex Christoph Bleidorn*1,2, Inken Kruse3, Sylvia Albrecht1,4 and Thomas Bartolomaeus1 Address: 1Animal Systematics and Evolution, Institute for Biology, Zoology, Free University Berlin, Koenigin-Luise-Str. 1-3, D-14195 Berlin, Germany, 2Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht- Strasse 24-25, Haus 26, D-14476 Potsdam-Golm, Germany, 3Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, Florida, USA and 4Institute for Zoo and Wildlife Research, 10252 Berlin, Germany Email: Christoph Bleidorn* - [email protected]; Inken Kruse - [email protected]; Sylvia Albrecht - [email protected]; Thomas Bartolomaeus - [email protected] * Corresponding author Published: 15 June 2006 Received: 20 February 2006 Accepted: 15 June 2006 BMC Evolutionary Biology 2006, 6:47 doi:10.1186/1471-2148-6-47 This article is available from: http://www.biomedcentral.com/1471-2148/6/47 © 2006 Bleidorn et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Polychaetes assigned as Scoloplos armiger (Orbiniidae) show a cosmopolitan distribution and have been encountered in all zoogeographic regions. Sibling S. armiger-like species have been revealed by recent studies using RAPDs and AFLP genetic data. We sequenced a ~12 kb fragment of the Scoloplos cf. armiger mitochondrial genome and developed primers for variable regions including the 3' end of the cox3 gene, trnQ, and most of nad6. A phylogenetic analysis of this 528-nucleotide fragment was carried out for S. armiger-like individuals from the Eastern North Atlantic as well as Pacific regions. The aim of this study is to test the cosmopolitan status, as well as to clarify the systematics of this species complex in the Eastern North Atlantic, while using a few specimens from the Pacific Ocean for comparision. Results: Phylogenetic analysis of the cox3-trnQ-nad6 data set recovered five different clades of Scoloplos cf. armiger. The fragment of the mitochondrial genome of Scoloplos cf. armiger is 12,042 bp long and contains 13 protein coding genes, 15 of the 22 expected tRNAs, and the large ribosomal subunit (rrnl). Conclusion: The sequenced cox3-trnQ-nad6 fragment proved to be very useful in phylogenetic analyses of Scoloplos cf. armiger. Due to its larger sampling scale this study goes beyond previous analyses which used RAPD and AFLP markers. The results of this study clearly supports that Scoloplos armiger represents a species complex and not a cosmopolitan species. We find at least two S. armiger-like species within the Pacific region and three different S. armiger-like species in the North Atlantic. Implications for the taxonomy and the impact on ecological studies are discussed. Background dominant species in ecological surveys in different marine Polychaetes assigned as Scoloplos armiger are common as habitats. Benthic surveys have shown that S. armiger rep- Page 1 of 13 (page number not for citation purposes) BMC Evolutionary Biology 2006, 6:47 http://www.biomedcentral.com/1471-2148/6/47 resents one of the dominant macrofauna species in a Nor- invasive sabellid Sabella spallanzanii was investigated wegian fjord [1], in a Portuguese estuary [2], and in the using nuclear markers [27] and human introduction to Peter the Great Bay in the Sea of Japan [3]. Besides its wide Australia due to ballast water has been suggested for this ranging distribution, S. armiger also plays a more or less polychaete. The cosmopolitan status of Hesionides areneria important role in recent ecological studies. It has been (Hesionidae) was confirmed using RAPD markers [28], identified as a possible intermediate host for the flatfish nevertheless it cannot be ruled out that lack of differences nematode Cucullanus heterochrous [4] and the population in the band pattern of RAPDs is due to primer choice. In dynamics of S. armiger and its predator Nephtys hombergii contrast to this, the cosmopolitan status of another hesio- (Nephtyidae) on intertidal flats in the Netherlands' part of nid (Hesionides gohari) was not supported by RAPD data the Wadden Sea are well studied [5]. [29]. Scoloplos armiger (Orbiniidae) has been reported to show Interestingly, none of these studies used mitochondrial a cosmopolitan distribution and has been encountered in markers which are commonly used for phylogeographic all zoogeographic regions [6,7] where it is present from studies in other animal groups [30]. This might be due to the intertidal to the subtidal [8,9]. In the North Sea region the lack of suitable primers for the amplification of varia- it is one of the most common polychaetes and a direct ble regions of the mitochondrial genome. Although many development in egg cocoons was observed at many inter- polychaetes are recorded from different zoogeographic tidal flats [8]. In additional to these well known and eye- regions, truly cosmopolitan species seem to be rare, and in catching cocoons, free swimming pelagic larvae of these many cases taxonomy is unable to distinguish between worms have been reported from the North Sea near the morphologically similar taxa [31]. It is supposed that island of Helgoland, Germany [10]. widely distributed species are frequently being found to consist of distinguishable subspecies or siblings when For many marine invertebrate species a worldwide distri- examined in sufficient detail [12]. bution has been reported. At least four hypotheses can reasonably explain such a distribution pattern; (a) truly In a series of papers it has been shown with RAPD data, cosmopolitan species, (b) cosmopolitan morphospecies AFLPs, cross-breeding experiments and investigation of which correspond to genetically distinct species [11,12], the sperm morphology, that different developmental (c) poor taxonomic understanding of a taxon, causing traits of Scoloplos armiger collected near the island of Sylt "the cosmopolitan syndrome" [13-15] and (d) cosmopol- (Germany) belong to two distinct Scoloplos species [32- itans where the current range distribution is the result of 34]. This means that two sympatric sibling species of Scol- human introductions. An example for the latter is the reef- oplos cf. armiger occur in the North Sea: one living in the building serpulid Ficopomatus enigmaticus which can be intertidal with egg cocoons and one living subtidally with found in brackish waters of warm-temperate regions all pelagic larvae. over the world, and which is supposed to be distributed through human shipping [16]. However, most reports of The aim of the present study is to investigate the status of cosmopolitan distributional ranges of marine invertebrate different Scoloplos cf. armiger populations in the Northern species after application of molecular methods turned out East Atlantic (see Fig. 1 for collection sites) and the North- to be the result of an over-conservative taxonomy [17-19]. ern East Pacific using mitochondrial markers. For this pur- pose we sequenced a 12 kb fragment of the mitochondrial Among marine invertebrates, polychaete annelids have a genome of Scoloplos cf. armiger to develop primers for a high frequency of cosmopolitan species [20,21]. Polycha- variable mitochondrial region. Our present study gives no etes like Owenia fusiformis (Oweniidae), Sternaspis scutata support for a cosmopolitan distribution of Scoloplos cf. (Sternaspidae) and Scoloplos armiger (Orbiniidae) are armiger and phylogenetic analyses of the investigated pop- recorded from all oceans in different depths and nearly all ulations reveal five distinct reciprocal monophyletic temperate regions [7,15,22]. However O. fusiformis later clades of Scoloplos cf. armiger. has been found to consist of more than one species [23]. Results Only a few genetic studies investigated such "cosmopoli- Genome organisation, base composition, and codon usage tan" polychaetes and most of them did not use discrete of the mitochondrial genome of Scoloplos cf. armiger nucleotide data. RAPDs and ITS sequence data confirmed The fragment of the mitochondrial genome of Scoloplos cf. the amphi-Atlantic distribution pattern of the ctenodrillid armiger individual SI14 is 12,042 bp long and contains 13 Ctenodrilus serratus [24]. The worldwide distributed Petitia protein coding genes, 16 of the 22 expected tRNAs, and amphophthalma (Syllidae) has been investigated with the large ribosomal subunit (rrnl). As in the case for all RAPD markers [25,26] which do not support the cosmo- annelids so far studied all genes are transcribed from the politan status of this taxon. The phylogeography of the same strand. One difference found in the gene arrange- Page 2 of 13 (page number not for citation purposes) BMC Evolutionary Biology 2006, 6:47 http://www.biomedcentral.com/1471-2148/6/47 MapFigure of collection1 sites in Europe Map of collection sites in Europe. Abbreviations are according to the labeling of individuals as given in Table 1: NT, Trond- heimsfjord (Norway); NK, Kristiansand (Norway); GB,
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