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Molecular data support the existence of two species of the Antarctic fish genus Cryodraco (Channichthyidae)

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Abstract

Antarctic notothenioids represent one of the few strongly supported examples of adaptive radiation in marine fishes. The extent of population connectivity and structure is unknown for many species, thereby limiting our understanding of the factors that underlie speciation dynamics in this radiation. Here, we assess the population structure of the widespread species Cryodraco antarcticus and its sister species Cryodraco atkinsoni, whose taxonomic status is currently debated. Combining both population genetic and phylogenetic approaches to species delimitation, we provide evidence that C. atkinsoni is a distinct species. Our analyses show that C. atkinsoni and C. antarcticus are recently diverged sister lineages, and the two species differ with regard to patterns of population structure. A systematic and accurate account of species diversity is a critical prerequisite for investigations into the complex processes that underlie the history of speciation in the notothenioid adaptive radiation.

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References

  • Allcock AL et al (2011) Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep-Sea Res Part II 58:242–249

    Article  Google Scholar 

  • Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P (2013) Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30:239–243

    Article  CAS  PubMed  Google Scholar 

  • Balushkin AV (1996) Similarity of family Channichthyidae (Notothenioidei, Perciformes), with remarks on the species composition of the family and the description of a new species from the Kerguelen Archipelago. J Ichthyol 36:1–10

    Google Scholar 

  • Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7:1255–1256

    CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Cziko PA, Cheng C-HC (2006) A new species of nototheniid (Perciformes: Notothenioidei) fish from McMurdo Sound. Antarct Copeia 2006:752–759

    Article  Google Scholar 

  • Damerau M, Matschiner M, Salzburger W, Hanel R (2012) Comparative population genetics of seven notothenioid fish species reveals high levels of gene flow along ocean currents in the southern Scotia Arc. Antarct Polar Biol 35:1073–1086

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710

    Article  CAS  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Eastman JT (1985) The evolution of neutrally buoyant notothenioid fishes: their specializations and potential interactions in the Antarctic marine food web. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 430–436

    Chapter  Google Scholar 

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

    Google Scholar 

  • Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107

    Article  Google Scholar 

  • Eastman JT, Clarke A (1998) A comparison of adaptive radiations of Antarctic fish with those of non-Antarctic fish. In: Di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer, Milano, pp 3–26

    Chapter  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Eytan RI, Hellberg ME (2010) Nuclear and mitochondrial sequence data reveal and conceal different demographic histories and population genetic processes in Caribbean reef fishes. Evolution 64:3380–3397

    Article  CAS  PubMed  Google Scholar 

  • Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flot JF (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Resour 10:162–166

    Article  CAS  PubMed  Google Scholar 

  • Fraser CI, Nikula R, Ruzzante DE, Waters JM (2012) Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends Ecol Evol 27:462–471

    Article  PubMed  Google Scholar 

  • Hein J, Schierup MH, Wiuf C (2005) Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford University Press, Oxford

    Google Scholar 

  • Hubert N, Delrieu-Trottin E, Irisson J-O, Meyer C, Planes S (2010) Identifying coral reef fish larvae through DNA barcoding: a test case with the families Acanthuridae and Holocentridae. Mol Phylogenet Evol 55:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Andolfatto P, Huelsenbeck ET (2011) Structurama: Bayesian inference of population structure. Evol Bioinf Online 7:55

    Article  Google Scholar 

  • Hureau JC (1985) Nototheniidae. In: Fischer W, Hureau JC (eds) FAO species identification sheets for fishery purposes: Southern Ocean (Fishing areas 48, 58 and 88) (CCAMLR Convention Area), vol 2. FAO, Rome, pp 233–471

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Iwami T, Kock K-H (1990) Channichthyidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. J.L.B. Smith Institute of Ichthyology, Grahamstown, pp 381–399

    Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kearse M et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF (1995) Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Mol Phylogenet Evol 4:420–432

    Article  CAS  PubMed  Google Scholar 

  • Kock KH (1992) Antarctic fish and fisheries. Studies in polar research. Cambridge University Press, Cambridge

    Google Scholar 

  • Kock KH (2005) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, part I. Polar Biol 28:862–895

    Article  Google Scholar 

  • Kock K-H, Jones CD (2002) The biology of the icefish Cryodraco antarcticus Dollo, 1900 (Pisces, Channichthyidae) in the southern Scotia Arc (Antarctica). Polar Biol 25:416–424

    Google Scholar 

  • Kock KH, Jones CD (2005) Fish stocks in the southern Scotia Arc region—a review and prospects for future research. Rev Fish Sci 13:75–108

    Article  Google Scholar 

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

    Google Scholar 

  • La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338

    Article  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  CAS  PubMed  Google Scholar 

  • Lautredou A-C, Bonillo C, Denys 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 

  • Lopez JA, Chen WJ, Ortí G (2004) Esociform phylogeny. Copeia 2004:449–464

    Article  Google Scholar 

  • Marino I et al (2013) Evidence for past and present hybridization in three Antarctic icefish species provides new perspectives on an evolutionary radiation. Mol Ecol 22:5148–5161

    Article  CAS  PubMed  Google Scholar 

  • Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587

    Article  CAS  PubMed  Google Scholar 

  • Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the notothenioid adaptive radiation. Plos ONE 6. doi:10.1371/journal.pone.0018911

  • Miller RG (1993) A history and atlas of the fishes of the Antarctic Ocean. Foresta Institute for Ocean and Mountain Studies, Carson City

    Google Scholar 

  • Near TJ et al (2012) Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc Natl Acad Sci USA 109:3434–3439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norman JR (1938) Coast fishes. Part III. The Antarctic zone. Discov Rep 18:1–104

    Article  Google Scholar 

  • Papetti C, Pujolar JM, Mezzavilla M, La Mesa M, Rock J, Zane L, Patarnello T (2012) Population genetic structure and gene flow patterns between populations of the Antarctic icefish Chionodraco rastrospinosus. J Biogeogr 39:1361–1372

    Article  Google Scholar 

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  • Pegg GG, Sinclair B, Briskey L, Aspden WJ (2006) MtDNA barcode identification of fish larvae in the southern Great Barrier Reef-Australia. Sci Mar 70:7–12

    Article  CAS  Google Scholar 

  • Pons J et al (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond AJ (2003) Tracer, MCMC trace analysis package, 1.5 edn. http://beast.bio.ed.ac.uk/Tracer

  • Regan CT (1913) The Antarctic fishes of the Scottish National Antarctic Expedition. Trans R Soc Edinb 49:229–292

    Article  Google Scholar 

  • Regan CT (1914) Fishes. British Antarctic Terra Nova Expedition, 1910, natural history report. Zoology 1:1–54

    Google Scholar 

  • Reid NM, Carstens BC (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol 12:196

    Article  PubMed  PubMed Central  Google Scholar 

  • Rock J, Costa F, Walker D, North A, Hutchinson W, Carvalho G (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 

  • Rutschmann S, Matschiner M, Damerau M, Muschick M, Lehmann MF, Hanel R, Salzburger W (2011) Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol Ecol 20:4707–4721

    Article  PubMed  Google Scholar 

  • Shandikov GA, Eakin RR (2013) Pogonophryne neyelovi, a new species of Antarctic short-barbeled plunderfish (Perciformes, Notothenioidei, Artedidraconidae) from the deep Ross Sea. ZooKeys 296:59–77

  • Shandikov GA, Eakin RR, Usachev S (2013) Pogonophryne tronio, a new species of Antarctic short-barbeled plunderfish (Perciformes: Notothenioidei: Artedidraconidae) from the deep Ross Sea with new data on Pogonophryne brevibarbata. Polar Biol 36:273–289

    Article  Google Scholar 

  • Smith PJ, Steinke D, Dettai A, McMillan P, Welsford D, Stewart A, Ward RD (2012) DNA barcodes and species identifications in Ross Sea and Southern Ocean fishes. Polar Biol 35:1297–1310

    Article  Google Scholar 

  • Spodareva V, Balushkin A (2014) Description of a new species of plunderfish of genus Pogonophryne (Perciformes: Artedidraconidae) from the Bransfield Strait (Antarctica) with a key for the identification of species of the group “marmorata”. J Ichthyol 54:1–6

    Article  Google Scholar 

  • Steinke D, Zemlak TS, Hebert PD (2009) Barcoding Nemo: DNA-based identifications for the ornamental fish trade. PLoS ONE 4:e6300

    Article  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  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 

  • Vacchi M, La Mesa M (1997) Morphometric analysis of Cryodraco specimens (Notothenioidei: Channichthyidae) from Terra Nova Bay, Ross Sea. Cybium 21:363–368

    Google Scholar 

  • Valdez-Moreno M, Quintal-Lizama C, Gómez-Lozano R, del Carmen G-RM (2012) Monitoring an alien invasion: DNA barcoding and the identification of lionfish and their prey on coral reefs of the Mexican Caribbean. PLoS ONE 7:e36636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968

    Article  CAS  Google Scholar 

  • Waite ER (1916) Fishes Australasian Antarctic Expedition 1911–1914. Sci Rep Ser C Zool Bot 3:3–92

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Young EF et al (2015) Oceanography and life history predict contrasting genetic population structure in two Antarctic fish species. Evol Appl 8:486–509

    Article  PubMed  PubMed Central  Google Scholar 

  • Zane L et al (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:4499–4511

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Fieldwork was facilitated through the United States Antarctic Marine Living Resources Program and the officers and crew of the RV Yuzhmorgeologia, the 2004 ICEFISH cruise aboard the RVIB Nathaniel B. Palmer, and the 2008 IPY/CAML expedition aboard the RV Tangaroa funded by the New Zealand Government. Specimens and data collected by and made available through the New Zealand International Polar Year-Census of Antarctic Marine Life Project are gratefully acknowledged. Field and laboratory support was provided by H. W. Detrich, J. Kendrick, K.-H. Kock, K. L. Kuhn, and J. A. Moore. This research was funded from a NSF grant awarded to T.J.N. (PLR-1341661). All sequence alignment and analysis files used in this study have been archived on Zenodo (DOI:10.5281/zenodo.35673).

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Authors and Affiliations

  1. Ichthyology Unit, North Carolina Museum of Natural Sciences, 11 West Jones Street, Raleigh, NC, 27601, USA

    Alex Dornburg

  2. Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, 77553, USA

    Ron I. Eytan

  3. Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, 06520, USA

    Sarah Federman & Thomas J. Near

  4. Ezra Stiles College, Yale University, New Haven, CT, 06520, USA

    Jillian N. Pennington

  5. Museum of New Zealand Te Papa Tongarewa, PO Box 467, Wellington, New Zealand

    Andrew L. Stewart

  6. Antarctic Ecosystem Research Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, 92037, USA

    Christopher D. Jones

  7. Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA

    Thomas J. Near

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  1. Alex Dornburg
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Dornburg, A., Eytan, R.I., Federman, S. et al. Molecular data support the existence of two species of the Antarctic fish genus Cryodraco (Channichthyidae). Polar Biol 39, 1369–1379 (2016). https://doi.org/10.1007/s00300-015-1859-9

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