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Full Text in Pdf Format Vol. 8: 95–103, 2009 AQUATIC BIOLOGY Published online December 29 doi: 10.3354/ab00205 Aquat Biol OPENPEN ACCESSCCESS Molecular phylogenetics of pricklebacks and other percoid fishes from the Sea of Japan Yuri P. Kartavtsev1, 2,*, Svetlana N. Sharina1, Tadasuke Goto3, Olesya A. Rutenko2, Vladimir V. Zemnukhov1, Alexander A. Semenchenko2, Dmitri L. Pitruk1, Naoto Hanzawa3 1A.V. Zhirmunsky Institute of Marine Biology, FEB RAS, Vladivostok 690041, Russia 2Far Eastern State University, Vladivostok 690095, Russia 3Department of Biology, Faculty of Science, Yamagata University, Yamagata 990-8560, Japan ABSTRACT: Mitochondrial DNA of the Co-1 gene region was sequenced for 8 fish species (in total 17 sequences of at least 532 bp) from the far east of Russia and compared to 3 other perciform sequences, altogether comprising 20 perch-like fish sequences and 2 outgroup sequences (Cypriniformes). The analysis of the protein-coding Co-1 gene revealed a statistically substantiated bias in the (T+C):(A+G) content, confirming the basic findings on the pyrimidines-prunes ratio. The average scores of p-distances for different scales of the evolutionary history of the Co-1 gene revealed a pat- tern of increased nucleotide diversity at 4 different levels: (1) intraspecies, (2) intragenus, (3) intrafamily and (4) intraorder. The scores of the average p-distances of the 4 categories of compari- son were: (1) 0.11 ± 0.04%, (2) 1.87 ± 0.68%, (3) 12.67 ± 0.28%, and (4) 16.52 ± 0.10%, respectively (mean ± SE). These data support the concept that speciation in the order Perciformes in most cases follows a geographic mode through accumulation of numerous small genetic changes over a long time. The phylogenetic trees for 18 and 21 sequences of perch-like fishes together with 2 other fishes belonging to the ray-finned fishes (Actinopterygii) were developed using the Co-1 gene and 4 differ- ent analytical approaches: neighbour-joining (NJ), maximum likelihood (ML), Bayesian (BA) and maximum parsimony (MP). The analysis revealed a monophyletic origin for the representatives of the Stichaeidae, which was the principal percoid family investigated (86, 96 and 100% support in our NJ, ML and BA analyses, respectively). Species identification on a per individual basis or Co-1-based DNA barcoding was high. KEY WORDS: Co-1 · cytochrome c oxidase 1 · Mitochondrial DNA · Identification · Percoid Resale or republication not permitted without written consent of the publisher INTRODUCTION Very popular for such research are sequences of the cytochrome oxidase 1 (Co-1) and cytochrome b (Cyt-b) Mitochondrial DNA (mtDNA) is now widely used for genes, which are best suited for analyses from the spe- phylogenetic purposes for a wide range of taxa. Many cies up to the family level (Johns & Avise 1998, Hebert regions of mtDNA that code for protein genes or par- et al. 2004, Kartavtsev & Lee 2006). However, single- ticipate in regulation as the control region are used as gene approaches provide inadequate phylogenetic genetic markers for investigation of intra- and inter- data when applied to higher taxa (above the order species diversity. mtDNA is able to accumulate many level), a result of insufficient information capacity and base substitutions over a long period of time, providing homoplasy effects (Hillis et al. 1996). Another com- a comparative tool for taxonomic, evolutionary and plication in the successful application of mtDNA phylogenetic research (Nei 1987, Wallace 1992, Avise sequence data, as well as any other markers, is a vast 2000). Molecular phylogenetic approaches use se- variation in the degree of genetic diversity within quence diversities of a single gene, multiple genes or many taxa (Johns & Avise 1998, Hebert et al. 2004, the complete mitochondrial genome (mitogenome). Kartavtsev & Lee 2006). Thus, a simple distance-like *Email: [email protected] © Inter-Research 2009 · www.int-res.com 96 Aquat Biol 8: 95–103, 2009 ranking even among vertebrate animals is quite a com- Some fishes in the family Stichaeidae have been inves- plicated task. Nevertheless, the bulk of evidence dem- tigated by phylogeneticists (Ward et al. 2005, Ward & onstrates that sequence data, e.g. for Co-1 or Cyt-b, Holmes 2007, Radchenko et al. 2009). To our knowl- are a useful tool for species discrimination (as DNA edge, however, only a few representatives were com- barcoding tags) and very helpful for phylogenetic pared simultaneously by using sequence divergence at reconstructions, including numerous fish taxa (Avise Co-1. Promising results for percoids were obtained at 2000, Hebert et al. 2004, Kim et al. 2004, Ward et al. other loci, such as 12S, 16S rRNA and Cyt-b of mtDNA 2005, Kartavtsev & Lee 2006). Pooling data such as that definitely showed monophyly of some investi- p-distances (Nei & Kumar 2000), or their derivates, gated tribes and families in the order (Stepien et al. across different taxon levels gives repetitive support 1997, Reed et al. 2002, Orrell & Carpenter 2004, Kim et for an increase of genetic diversity starting at the al. 2004). Serious disagreements with current taxon- intraspecies level and up to higher taxonomic ranks omy were also found at several DNA markers (Craig & (Johns & Avise 1998, Hebert et al. 2004, Kartavtsev Hastings 2007, Radchenko et al. 2009). 2005, Ward et al. 2005, Kartavtsev & Lee 2006, Kartavt- During a BLAST search of NCBI GenBank (www. sev et al. 2007a,b). This positive and proportional dis- ncbi.nlm.nih.gov) based on the fish Pholidapus dybov- tance score increase along with a taxon rank increase skii, a reference sequence investigation for close prox- may be used as a helpful attribute in searching for the imity among Co-1 sequences revealed 1 hit with only a most common speciation mode, a geographic mode few mtDNA sequences, most of which are short partial (Ayala et al. 1974, Avise 2000). However, because of sequences. Nevertheless, our search for Co-1 provided the complexity of species criteria, distance data alone several quite long sequences for the gene (~650 bp), may give only a part of the necessary information for which allowed us to make a molecular taxonomic and discrimination among speciation modes (Kartavtsev et phylogenetic evaluation for perch-like fishes on this al. 2002, Kartavtsev 2005, Kartavtsev & Lee 2006). basis. However, taking into consideration the large The need for molecular genetic research in percoid diversity in the order Perciformes, which currently fish species becomes apparent when considering taxo- comprises 156 recent families, with 77 species in the nomic complications and population structure analysis. family Stichaeidae alone (Froese & Pauly 2009), the There are numerous taxonomic problems associated possibility of obtaining an absolutely reliable molecu- with many groups and certain perch-like species of lar phylogenetic topology for the whole order Perci- Perciformes (Nelson 2006), which is one of the largest formes, from Co-1, Cyt-b or any other single gene, fish orders. Most families in many suborders are not seems remote. currently definable in terms of shared derived charac- Here, we focus on the family Stichaeidae and discuss ters and thus may not be monophyletic. This is espe- 3 to 4 representatives of other percoid fish families by cially true for those species that have a low commercial molecular phylogenetic and taxonomic considerations value, like pricklebacks (Stichaeidae). For instance, using Co-1 sequence data. Two main questions were the family Stichaeidae has no consensus position in considered: (1) whether the family Stichaeidae is taxonomic revisions (e.g. Makushok 1986a,b, Nelson monophyletic, and (2) whether the nucleotide diversity 2006). However, in accordance with the Integrated at Co-1 supports the currently accepted intra-family Taxonomic Information System (IT IS: www.itis.gov/), and intra-genus divisions. it does hold such a position. Currently (17 December 2009), 6 genera are placed in the family Stichaeidae by the NCBI Taxonomic Browser (http://www.ncbi.nlm. MATERIALS AND METHODS nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Tree& id=30892&lvl=3&lin=f&keep=1&srchmode=1&unlock). In total, we sampled 17 white muscle tissue speci- Meanwhile, 41 genera were placed within the family mens of 8 percoid fish species sampled in 2005–2006: in an earlier version of FishBase (Froese & Pauly 2009), (1) Stichaeus grigorjewi (Herzenstein, 1890), (2) S. and 77 species of 38 genera are currently listed in the nozawae (Jordan & Snyder, 1902), (3) Ammodytes family Stichaeidae in a more recent version of FishBase hexapterus (Pallas, 1814), (4) Arctoscopus japonicus (Froese & Pauly 2009). Thus, it is obvious that much (Steindachner, 1881), (5) Chirolophis japonicus (Herzen- molecular taxonomy and phylogenetic research on stein, 1890), (6) Pholidapus dybowskii (Steindachner, Stichaeidae and other perch-like fish species remains 1881), (7) Opisthocentrus ocellatus (Tilesius, 1811), to be conducted. (8) O. tenuis Bean & Bean, 1897, and 2 specimens of a Many molecular marker investigations in perch-like single cyprinid species, Tribolodon brandtii (Dybowski, fishes with respect to phylogeny have been reported 1872) as an outgroup (Table 1). Muscle tissues were recently (Finnerty & Block 1995, Lydeard & Roe 1997, taken from all individuals, which were collected by gill Song et al. 1998, Reed et al. 2002, Kim et al. 2004). nets in April to September in Vostok Bay (132° 44’ Kartavtsev et al.: Molecular phylogenetics of pricklebacks 97 Table 1. GenBank accession numbers for Co-1 gene sequences and location The PCR reaction mixture (25 µl) con- of collections of the examined species. Alcohol-preserved specimens and sisted of 2.5 µl Ex-Taq buffer (TaKaRa), 1 voucher individuals were deposited in collections at the A.V. Zhirmunsky µl of F1-primer (20 pmol µl–1), 1 µl of R1- Institute of Marine Biology primer (20 pmol µl–1), 2 µl of dNTP mix- ture, 1 µl of template, 0.5 µl of Taq poly- No. Accession Species and specimen Date merase (5 units µl–1) and 17.4 µl of distilled number (dd/mm/yy) water.
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