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DNA barcodes and species identifications in Ross Sea and Southern Ocean fishes

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Abstract

The Southern Ocean occupies about 10 % of the world’s oceans but has low species richness with only ~1.5 % of the marine fishes. Within the Southern Ocean, the Ross Sea region is one of the least exploited sea areas in the world, but is subject to commercial fishing. The fauna are not well known, and preliminary IPY molecular studies have indicated that species diversity has been underestimated in this region. DNA barcodes of fishes from the Ross Sea region were compared with barcodes of fishes from the Atlantic and Indian Ocean sectors of the Southern Ocean. Barcoding resolved 87.5 % of 112 species that typically exhibited high inter-specific divergences. Intra-specific divergence was usually low with shared haplotypes among regions. The Zoarcid Ophthalmolycus amberensis showed shallow divergences (0.1 %) within the Ross Sea and Australian Antarctic Territory but high inter-region divergence (2 %), indicative of cryptic species. Other potential cryptic species with high intra-specific divergences were found in Notolepis coatsi and Gymnoscopelus bolini. In contrast, several taxa showed low inter-specific divergences and shared haplotypes among morphological species. COI provided limited phylogenetic resolution of the genera Pogonophryne and Bathydraco. Trematomus loennbergii and T. lepidorhinus shared COI haplotypes, as previously noted in other regions, as did Cryodraco antarcticus and C. atkinsoni. There was a marked lack of congruence between morphological descriptions and COI divergences among the Ross Sea liparids with shallow or zero divergences among recently described species. Barcodes for the Ross Sea fishes highlighted several initial misidentifications that were corrected when specimens were re-examined.

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References

  • Allcock I, Brierley AS, Thorpe J, Rodhouse PG (1997) Restricted geneflow and evolutionary divergence between geographically separated populations of the Antarctic octopus Pareledone turqueti. Mar Biol 129:97–102

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, p 477

    Google Scholar 

  • Balushkin A, Eakin R (1998) A new toad plunderfish Pogonophryne fusca sp. nova (Fam. Artedidraconidae: Notothenioidei) with notes on species composition and species groups in the genus Pogonophryne Regan. J Ichthyol 38:574–579

    Google Scholar 

  • Brierley AS, Rodhouse PG, Thorpe JP, Clarke MR (1993) Genetic evidence of population heterogeneity and cryptic speciation in the ommastrephid squid Martialia hyadesi from the Patagonian Shelf and Antarctic Polar Front Zone. Mar Biol 16:593–602

    Article  Google Scholar 

  • Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crust Biol 29:96–110

    Article  Google Scholar 

  • Chen WJ, Bonillo C, Lecointre G (1998) Phylogeny of the Channichthyidae (Notothenioidei, Teleostei) based on two mitochondrial genes In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer-Verlag Italia, Milano, 1998. ISBN 88 470 0028 9

  • Clark AM (2000) Benthic organisms and environmental variability in Antarctica: responses to seasonal, decadal and long-term change. Ocean Polar Res 23:433–440

    Google Scholar 

  • Clarke A, Johnston N (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol Ann Rev 41:47–114

    Google Scholar 

  • De Broyer C, Danis B (2010) How many species in the Southern Ocean? Towards a dynamic inventory of the Antarctic marine species. Deep Sea Res II 58:5–17

    Article  Google Scholar 

  • Derome N, Chen WJ, Dettai A, Bonillo C, Lecointre G (2002) Phylogeny of Antarctic dragonfishes (Bathydraconidae, Notothenioidei, Teleostei) and related families based on their anatomy and two mitochondrial genes. Mol Phylogenet Evol 24:139–152

    Article  PubMed  CAS  Google Scholar 

  • DeSalle R (2006) Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Cons Biol 20:1545–1547

    Article  Google Scholar 

  • Dettai A et al (2011a) The actinopterygian diversity of the CEAMARCcruises: barcoding and molecular taxonomy as a multi level tool for new findings. Deep Sea Res II 58:250–263

    Article  CAS  Google Scholar 

  • Dettai A et al (2011b) Barcoding and molecular systematics of the benthic and demersal organisms of the CEAMARC survey. Polar Sci 5:298–312

    Article  Google Scholar 

  • DeVries A, Steffensen J (2005) The Arctic and Antarctic polar marine environments. Physiol Fish 22:1–24

    Article  Google Scholar 

  • Duhamel G, Hautecoeur M, Dettai A, Causse R, Pruvost P, Busson F, Couloux, Koubbi P, Williams R, Ozouf-Costaz C, Nowara G (2010) Liparids from the Eastern sector of Southern Ocean and first information from molecular studies. Cybium 34:319–343

    Google Scholar 

  • Eakin R (1990) Artedidraconidae. In: Gon O, Heemstra P (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 332–356

    Google Scholar 

  • Eakin R, Eastman J (1998) New species of Pogonophryne (Pisces, Artedidraconidae) from the Ross Sea, Antarctica. Copeia 1998:1005–1009

    Article  Google Scholar 

  • Eakin RR, Eastman JT, Near TJ (2009) A new species and a molecular phylogenetic analysis of the Antarctic fish genus Pogonophryne (Notothenioidei: Artedidraconidae). Copeia 2009:705–713

    Article  Google Scholar 

  • Eastman J (1993) Antarctic fish biology: evolution in a unique environment. Academic Press, San Diego, p 322

    Google Scholar 

  • Eastman JT (2000) Antarctic notothenioid fishes as subjects for research in evolutionary biology. Antarct Sci 12:276–287

    Article  Google Scholar 

  • Eastman J, McCune A (2000) Fishes on the Antarctic continental shelf: evolution of a marine species flock? J Fish Biol 57:84–102

    Google Scholar 

  • Eschmeyer WN, Fricke R (2009) Catalog of Fishes electronic version (9 September 2009). http://research.calacademy.org/ichthyology/catalog/fishcatmain.asp

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Frankham R, Ballou J, Briscoe D (2004) A primer of conservation genetics. Cambridge University Press, Cambridge, p 234

    Book  Google Scholar 

  • Gon O, Heemstra P (1990) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, p 462

    Google Scholar 

  • Grant RA, Griffiths H, Steinke D, Linse K (2011) Antarctic DNA barcoding; a drop in the ocean? Polar Biol 34:775–780

    Article  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 Biol Sci 270:S96–S99

    Article  CAS  Google Scholar 

  • Held C, Leese F (2007) The utility of fast evolving molecular markers for studying speciation in the Antarctic benthos. Polar Biol 30:513–521

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the drake passage in the Southern Ocean. J Hered 99:137–148

    Article  PubMed  CAS  Google Scholar 

  • Ivanova NV, deWaard JR, Heber PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002

    Article  CAS  Google Scholar 

  • Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548

    Article  CAS  Google Scholar 

  • Janko K, Lecointre G, DeVries D, Couloux A, Cruaud C, Marshall C (2007) Did glacial advances during the Pleistocene influence differently the demographic histories of benthic and pelagic Antarctic shelf fishes? Inferences from intraspecific mitochondrial and nuclear DNA sequence diversity. BMC Evol Biol 7:220

    Article  PubMed  Google Scholar 

  • Janosik AM, Halanych KM (2010) Unrecognized Antarctic biodiversity: a case study with Odontaster (Odontasteridae; Asteroidea). J Int Comp Biol 50:981–992

    Article  Google Scholar 

  • Janosik AM, Mahon AR, Halanych KM (2011) Evolutionary history of Southern Ocean seastar species across the Drake Passage, and the discovery of 2 species of Odontaster (Odontasteridae; Asteroidea). Polar Biol 34:575–586

    Article  Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Nat Acad Sci 78:454–458

    Article  PubMed  CAS  Google Scholar 

  • Kuhn KL, Gaffney PM (2008) Population subdivision in the Antarctic toothfish (Dissostichus mawsoni) revealed by mitochondrial and nuclear single nucleotide polymorphisms (SNPs). Antarct Sci 20:327–338

    Google Scholar 

  • Kuhn KL, Near J (2009) Phylogeny of trematomus (Notothenioidei: Nototheniidae) inferred from mitochondrial and nuclear gene sequences. Antarct Sci 21:565–570

    Article  Google Scholar 

  • La Mesa M, Vacchi M, Iwami T, Eastman JT (2002) Taxonomic studies of the Antarctic icefish genus Cryodraco Dollo, 1900 (Nototheniodei: Channichthidae). Polar Biol 25:384–390

    Google Scholar 

  • Lautrédou A-C, Bonillo C, Denis G, Cruaud C, Ozouf-Costaz C, Lecointre G, Dettai A (2010) Molecular taxonomy and identification within the Antarctic genus Trematomus (Notothenioidei, Teleostei): how valuable is barcoding with COI? Polar Sci 4:333–352

    Article  Google Scholar 

  • Lecointre G, Gallut C, Bonillo C, Couloux A, Ozouf-Costaz C, Dettai A (2011) The Antarctic Fish Genus Artedidraco is paraphyletic (Teleostei, Notothenioidei, Artedidraconidae). Polar Biol 34:1135–1145

    Article  Google Scholar 

  • Long DJ (1994) Quaternary colonization or Paleogene persistence?: historical biogeography of skates (Chondrichthys: Rajidae) in the Antarctic ichthyofauna. Palaeobiology 20:215–228

    Google Scholar 

  • Meyer C, Paulay G (2005) DNA Barcoding: error rates based on comprehensive sampling. PLoS Biol 3:2229–2238

    CAS  Google Scholar 

  • Møller P, Nielsen, Anderson M (2005) Systematics of polar fishes. Fish Physiol 22:25–78

    Article  Google Scholar 

  • Moritz C, Cicero C (2004) DNA barcoding: promises and pitfalls. PLoS Biol 2:1529–1531

    Article  CAS  Google Scholar 

  • Near TJ, Pesavento JJ, Cheng CH (2003) Mitochondrial DNA, morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae). Mol Phylogenet Evol 28:87–98

    Article  PubMed  CAS  Google Scholar 

  • Near TJ, Pesavento JJ, Cheng CC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol Phylogenet Evol 32:881–891

    Article  PubMed  CAS  Google Scholar 

  • Orsi AH, Whitworth T, Nowlin WD (1995) On the meridional extent and fronts of the Antarctic circumpolar current. Deep Sea Res 42:641–673

    Article  Google Scholar 

  • Parker RW, Paige KN, DeVries AL (2002) Genetic variation among populations of the Antarctic toothfish: evolutionary insights and implications for conservation. Polar Biol 25:256–261

    Google Scholar 

  • Pollard D, DeConto RM (2009) Modelling West Antarctic ice sheet growth and collapse through the past five million years. Nature 458:329–333

    Article  PubMed  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) The barcode of life database. Mol Ecol Notes 7:355–364

    Article  PubMed  CAS  Google Scholar 

  • Ritchie PA, Bargelloni L, Meyer A, Taylor JA, MacDonald JA, Lambert DM (1996) Mitochondrial phylogeny of trematomid fishes (Nototheniidae, Perciformes) and the evolution of antarctic fish. Mol Phylogenet Evol 5:383–390

    Article  PubMed  CAS  Google Scholar 

  • Rock J, Costa FO, Walker DI, North AW, Hutchinson WF, Carvalho GR (2008) DNA barcodes of fish of the Scotia Sea, Antarctica indicate priority groups for taxonomic and systematics focus. Antarct Sci 20:253–262

    Article  Google Scholar 

  • Rubinoff D, Cameron S, Will K (2006) A genomic perspective on the shortcomings of mitochondrial DNA for “barcoding” identification. J Hered 97:581–594

    Article  PubMed  CAS  Google Scholar 

  • Sanchez S, Dettai A, Bonillo C, Ozouf-Costaz C, Detrich B, Lecointre G (2007) Molecular and morphological phylogenies of the Antarctic teleostean family Nototheniidae, with emphasis on the Trematominae. Polar Biol 30:155–166

    Article  Google Scholar 

  • Sevilla RG, Diez A, Noren M, Mouchel O, Jerome M, Verrez-Bagnis V, Van Pelt H, Favre KL, Krey G, Bautista JM (2007) Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Mol Ecol Notes 7:730–734

    Article  CAS  Google Scholar 

  • Shaw P, Arkhipkin A, Al-Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13:3293–3303

    Article  PubMed  CAS  Google Scholar 

  • Shearer T, Coffroth M (2008) Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Res 8:247–255

    Article  CAS  Google Scholar 

  • Smith PJ, Gaffney P (2005) Low genetic diversity in the Antarctic toothfish Dissostichus mawsoni observed with mitochondrial and intron DNA markers. CCAMLR Sci 12:43–51

    Google Scholar 

  • Smith PJ, McVeagh SM (2000) Allozyme and microsatellite DNA markers of toothfish population structure in the Southern Ocean. J Fish Biol 57:72–83

    Article  CAS  Google Scholar 

  • Smith PJ, Steinke D, McVeagh SM, Stewart AL, Struthers CD, Roberts CD (2008) Molecular analysis of Southern Ocean skates (Bathyraja) reveals a new species of Antarctic skate. J Fish Biol 73:1170–1182

    Article  CAS  Google Scholar 

  • Smith PJ, Steinke D, McMillan PJ, Stewart AL, McVeagh SM, Diaz de Astarloa JM, Welsford D, Ward RD (2011a) DNA barcoding highlights a cryptic species of grenadier (genus Macrourus) in the Southern Ocean. J Fish Biol 78:355–365

    Article  PubMed  CAS  Google Scholar 

  • Smith PJ, Steinke D, McMillan PJ, Stewart AL, Ward RD (2011b) DNA barcoding of morids (Actinopterygii, Moridae) reveals deep divergence in the anti tropical Halargyreus johnsonii but little distinction between Antimora rostrata and A. microlepis. Mitochondrial DNA 22(S1):21–26

  • Steinke D, Zemlak TS, Boutillier JA, Hebert PDN (2009) DNA barcoding of Pacific Canada’s fishes. Mar Biol 156:2641–2647

    Article  Google Scholar 

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

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thornhill DJ, Mahon AR, Norenburg JL, Halanych KM (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Mol Ecol 17:5104–5117

    Article  PubMed  CAS  Google Scholar 

  • Van de Putte AP, Van Houdt JKJ, Maes GE, Hellemans B, Collins MA, Volckaert FAM (2012) High genetic diversity and connectivity in a common mesopelagic fish of the Southern Ocean: the myctophid Electrona antarctica. Deep Sea Res II Top Stud Oceanogr 59–60:199–207

    Article  Google Scholar 

  • Ward RD (2009) DNA barcode divergence among species and genera of birds and fishes. Mol Ecol Res 9:1077–1085

    Article  CAS  Google Scholar 

  • Ward RD, Holmes B, O’Hara TD (2008) DNA barcoding discriminates echinoderm species. Mol Ecol Notes 8:1202–1211

    CAS  Google Scholar 

  • Ward RD, Hanner R, Hebert PDN (2009) The campaign to DNA barcode all fishes, FISH-BOL. J Fish Biol 74:329–356

    Article  PubMed  CAS  Google Scholar 

  • Waugh J (2007) DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29:188–197

    Article  PubMed  CAS  Google Scholar 

  • Wilson NG, Schrödl M, Halanych KM (2009) Ocean barriers and glaciation: explosive radiation of Pleistocene lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984

    Article  PubMed  Google Scholar 

  • Zane L, Marcato S, Bargelloni L, Bortolotto E, Papetti C, Simonato M, Varotto V, Patarnello T (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:4499–4511

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to the New Zealand Ministry of Fisheries and CCAMLR Scientific Observers, and to the Australian Fisheries Management Authority observers for the collection of specimens in the commercial fisheries in the Ross Sea region, the Australian Antarctic Territory, and the Indian Ocean. Additional Ross Sea IPY specimens were collected and identified by Peter McMillan and Andrew Stewart aboard the NIWA Research vessel Tangaroa. Peter Smith, Peter McMillan, and Andrew Stewart were supported by the New Zealand Government under the NZ International Polar Year-Census of Antarctic Marine Life Project and acknowledge the Ministry of Fisheries Science Team and Ocean Survey 20/20 CAML Advisory Group (Land Information New Zealand, Ministry of Fisheries, Antarctica New Zealand, Ministry of Foreign Affairs and Trade, and National Institute of Water and Atmospheric Research Ltd.). D. Steinke and laboratory analyses of sequences generated at the Canadian Centre for DNA Barcoding (CCDB) were supported by funding of the Alfred P. Sloan Foundation to MarBOL and by the Government of Canada through Genome Canada, through the Ontario Genomics Institute (2008-0GI-ICI-03). Preservation and storage costs for voucher specimens from the Ross Sea registered into the Museum of New Zealand Te Papa Tongarewa were provided by the Te Papa Collection Development programme. The collection and study of the East Antarctic specimens from the CAML-CEAMARC cruises of the RSV Aurora Australis and the TRV Umitaka Maru (IPY project no. 53) were supported by the Australian Antarctic Division, the Japanese Science Foundation, the French polar institute IPEV (ICOTA and REVOLTA programs), the CNRS, the MNHN, and the ANR (White Project ANTFLOCKs USAR no. 07-BLAN-0213-01 directed by Guillaume Lecointre). We are grateful to Anton Van de Putte (Leuven, Belgium), Olly Berry, and Sharon Appleyard (Hobart, Australia), and two anonymous referees for constructive comments on the manuscript.

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300_2012_1173_MOESM1_ESM.xls

Appendix 1 Southern Ocean fishes barcoded listed by Species, Specimen Reference Number, GenBank Accession Number, Bold Process Number, and Institute storing specimens. The list excludes published data on Macrourus, available in Smith et al. (2011) (XLS 240 kb)

300_2012_1173_MOESM2_ESM.pdf

Appendix 2 COI relationships among the Artedidraconidae (154 specimens, including those identified to genus level only) from the Southern Ocean; unrooted ML tree. The scale bar represents an interval of the K2P model; numbers at nodes are bootstrap percentages (>75%). Sequence numbers represent BOLD Process Number, GenBank Accession Number, followed by Registration Number, and species name (PDF 37 kb)

300_2012_1173_MOESM3_ESM.pdf

Appendix 3 COI relationships among Trematomus specimens (181 specimens, including those identified to genus level only); unrooted ML tree. The scale bar represents an interval of the K2P model; numbers at nodes are bootstrap percentages (>75%). Sequence numbers represent BOLD Process Number, GenBank Accession Number, followed by Registration Number, and species name (PDF 42 kb)

300_2012_1173_MOESM4_ESM.pdf

Appendix 4 COI relationships among the Bathydraconidae (168 specimens, including those identified to genus level only) from the Southern Ocean; unrooted ML tree. The scale bar represents an interval of the K2P +G model; numbers at nodes are bootstrap percentages (>75%). Sequence numbers represent BOLD Process Number, GenBank Accession Number, followed by Registration Number, and species name (PDF 39 kb)

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Smith, P.J., Steinke, D., Dettai, A. et al. DNA barcodes and species identifications in Ross Sea and Southern Ocean fishes. Polar Biol 35, 1297–1310 (2012). https://doi.org/10.1007/s00300-012-1173-8

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