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Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula

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Abstract

The evolution of the marine benthic fauna of Antarctica has been shaped by geological and climatic atmospheric factors such as the geographic isolation of the continent and the subsequent installation of the Antarctic Circumpolar Current (ACC). Despite this isolation process, strong biogeographic links still exist between marine fauna from the Antarctic Peninsula and southern South America. Recent studies in different taxa have shown, for example, that shallow benthic organisms with long larval stages maintained contact after the physical separation of the continents and divergence may be associated with the intensification of the ACC in the late Miocene—early Pliocene. In this context, here we performed phylogenetic reconstructions and estimated the level of molecular divergence between congeneric species of Harpagifer, a marine notothenioid from the Antarctic Peninsula (Harpagifer antarcticus) and Patagonia (H. bispinis) using the mitochondrial control region. Phylogenies were reconstructed using Maximum Parsimony and Bayesian Inference, while the divergence time of H. antarcticus and H. bispinis was estimated following a relaxed Bayesian approach and assuming a strict molecular clock hypothesis. According to our estimation, the divergence between H. bispinis and H. antarcticus is more recent than expected if it was associated with the intensification of the ACC during the mid to late Miocene. We propose that climatic and oceanographic changes during the coldest periods of the Quaternary (i.e., Great Patagonian Glaciation, 1–0.9 Ma) and the northward migration of the Antarctic Polar Front may have assisted the colonization of southern South America by Harpagifer, from the Antarctic Peninsula via the Scotia Arc Islands.

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References

  • Aljanabi S, Martínez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucl Acids Res 25:4692–4693

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arntz W, Thatje S, Gerdes D, Gili J-M, Gutt J, Jacob U, Montiel A, Orejas C, Teixidó N (2005) The Antarctic-Magellan connection: macrobenthos ecology on the shelf and upper slope, a progress report. Sci Mar 69(Suppl 2):237–269

  • Aronson R, Thatje S, Clarke A, Peck L, Blake D, Wilga C, Seibel B (2007) Climate change and invisibility of the Antarctic benthos. Annu Rev Ecol Evol S 38:129–154

    Article  Google Scholar 

  • Bargelloni L, Ritchie P, Patarnello T, Battaglia B, Lambert D, Meyer A (1994) Molecular evolution at subzero temperature: mitochondrial and nuclear phylogenies of fishes from Antarctica (Suborden Notothenioidei), and the evolution of antifreeze glycopeptides. Mol Biol Evol 11(6):854–863

    CAS  PubMed  Google Scholar 

  • Bargelloni L, Marcato S, Zane L, Patarnello T (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to antarctic fish evolution and biogeography. Syst Biol 49(1):114–129

    Article  CAS  PubMed  Google Scholar 

  • Barker P, Thomas E (2004) Origin, signature and palaeoclimatic influence of the Antarctic Circumpolar Current. Earth Sci Rev 66:143–162

    Article  Google Scholar 

  • Barker P, Filipelli G, Florindo F, Martin E, Scher H (2007) Onset and role of the Antarctic Circumpolar Current. Deep-Sea Res Pt II 54:2388–2398

    Article  Google Scholar 

  • Brodeur J, Calvo J, Clarke A (2003) Myogenic cell cycle duration in Harpagifer species with sub-Antarctic and Antarctic distributions: evidence for cold compensation. J Exp Biol 206:1011–1016

    Article  PubMed  Google Scholar 

  • Chen W, 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, Milano, pp 287–298

    Chapter  Google Scholar 

  • Cheng C-HC (1998) Origin and mechanism of evolution of antifreeze glycoproteins in polar fishes. In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer, Milano, pp 311–328

    Chapter  Google Scholar 

  • Cheng C-HC, Detrich W (2007) Molecular ecophysiology of Antarctic notothenioid fishes. Philos T R Soc B 362:2215–2232

    Article  CAS  Google Scholar 

  • Cheng C-HC, DeVries A (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold water fishes. In: di Prisco G (ed) Life under extreme conditions. Springer, Berlin, pp 1–14

    Chapter  Google Scholar 

  • Cheng C-HC, Chen L, Near T, Jin Y (2003) Functional antifreeze glycoprotein genes in temperate-water new Zealand nototheniid fish infer an Antarctic evolutionary origin. Mol Biol Evol 20(11):1897–1908

    Article  CAS  PubMed  Google Scholar 

  • Clark M, Clarke A, Cockell C, Convey P, Detrich HW, Fraser K, Johnston I, Methe B, Murray A, L Peck, Römish K, Rogers A (2004) Antarctic genomics. Comp Funct Genom 5:230–238

    Article  CAS  Google Scholar 

  • Clark P, Archer D, Pollard D, Blum J, Rial J, Brovkin V, Mix A, Pisias N, Roy M (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quat Sci Rev 25:3150–3184

    Article  Google Scholar 

  • Clarke A, Crame JA (1997) Diversity, latitude and time: patterns in the shallow sea. In: Ormond RFG, Gage JD, Angel MV (eds) Marine biodiversity: causes and consequences. Cambridge University Press, Cambridge, pp 122–147

    Chapter  Google Scholar 

  • Clarke A, Johnston I (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11(5):212–218

    Article  CAS  PubMed  Google Scholar 

  • Clarke A, Barnes D, Hodgson D (2005) How isolated is Antarctica? Trends Ecol Evol 1:1–3

    Article  Google Scholar 

  • Crame JA (1999) An evolutionary perspectiva on marine faunal connections between southernmost south America and Antarctica. Sci Mar 63(Suppl 1):1–14

  • Dalziel IW, Lawver L, Pearce J, Barker P, Hastie A, Barfod D, Schenke H-W, Davis M (2013) A potential barrier to deep Antarctic circumpolar flow until the late Miocene? Geology 41:947–950

    Article  CAS  Google Scholar 

  • DeConto RM, Pollard D (2003) Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2. Nature 421:245–249

    Article  CAS  PubMed  Google Scholar 

  • Derome N, Chen W, 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  CAS  PubMed  Google Scholar 

  • Díaz A, Féral J-P, David B, Saucède T, Poulin E (2011) Evolutionary pathways among shallow and deep sea echinoids of the genus Sterechinus in the Southern Ocean. Deep-Sea Res Pt II 58(1–2):205–211

    Article  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Ho S, Phillips M, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4(5):699–710

    Article  CAS  Google Scholar 

  • Duhamel G, Hulley P-A, Causse R, Koubbi P, Vacchi M, Pruvost P, Vigetta S, Irisson J-O, Mormède S, Belchier M, Dettaï A, Detrich W, Gutt J, Jones CD, Kock K-H, Lopez LJ, Van de Putte A (2014) Chapter 7. Biogeographic patterns of fish. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz Cd’ et al (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 327–361

  • Eagles G, Livermore R (2002) Opening history of Powell Basin, Antarctic Peninsula. Mar Geol 185:195–205

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Filatov DA (2002) ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624

    Article  CAS  Google Scholar 

  • Flower B, Kennett J (1994) The middle Miocene climatic transition: east Antarctic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeogr Palaeocl 108:537–555

    Article  Google Scholar 

  • Fraser C, Nikula R, Spencer H, Waters J (2009) Kelp genes reveal effects of subantarctic sea ice during the last glacial maximum. P Natl Acad Sci USA 106(9):3249–3253

    Article  CAS  Google Scholar 

  • Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253:769–778

    Article  PubMed  Google Scholar 

  • Gersonde R, Crosta X, Abelmann A, Armand L (2005) Sea-surface temperature and sea ice distribution of the Southern Ocean at the EPILOG last glacial maximum—a circum-Antarctic view based on siliceous microfossil records. Quat Sci Rev 24:869–896

    Article  Google Scholar 

  • González-Wevar C, Nakano T, Cañete J, Poulin E (2010) Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean. Mol Phylogenet Evol 56:115–124

    Article  PubMed  Google Scholar 

  • González-Wevar C, Díaz A, Gérard K, Cañete J, Poulin E (2012) Divergence time estimations and contrasting patterns of genetic diversity between Antarctic and southern South America benthic invertebrates. Rev Chil Hist Nat 85:445–456

    Article  Google Scholar 

  • Griffiths H, Barnes D, Linse K (2009) Towards a generalized biogeography of the Southern Ocean benthos. J Biogeogr 36:162–177

    Article  Google Scholar 

  • Helmuth B, Veit R, Holberton R (1994) Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting. Mar Biol 120:421–426

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos T R Soc B 359:183–195

    Article  CAS  Google Scholar 

  • Hureau J (1990) Harpagiferidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 357–363

    Google Scholar 

  • Janko K, Marshall C, Musilová Z, Van Houdt J, Couloux A, Cruaud C, Lecointre G (2011) Multilocus analyses of an Antarctic fish species flock (Teleostei, Notothenioidei, Trematominae): phylogenetic approach and test of the early-radiation event. Mol Phylogenet Evol 60:305–316

    Article  PubMed  Google Scholar 

  • Johnston I, Vieira V, Fernandez DA, Abercromby M, Brodeur J, Peck L, Calvo J (2002) Muscle growth in polar fish: a study of Harpagifer species with sub-Antarctic and Antarctic distributions. Fish Sci 68:1023–1028

    Google Scholar 

  • Kemp A, Grigorov I, Pearce R, Garabato N (2010) Migration of the Antarctic Polar Front through the mid-Pleistocene transition: evidence and climatic implications. Quat Sci Rev 29:1993–2009

    Article  Google Scholar 

  • Kock K, Kellermann A (1991) Reproduction in Antarctic notothenioid fish. Rev Antarct Sci 3(2):125–150

    Google Scholar 

  • Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompson J, Gibson T, Higgins D (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lawver L, Gahagan L, Campbell D (2003) Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeogr Palaeocl 198:11–37

    Article  Google Scholar 

  • Lear C, Elderfield H, Wilson P (2000) Cenozoic deep-sea temperatures and global ice volumes from Mg/Ca in benthic foraminiferal calcite. Science 287:269–272

    Article  CAS  PubMed  Google Scholar 

  • Lewis A, Marchant D, Ashworth A, Hedena L, Hemming S, Johnson J, Leng M-J, Machlus M, Newton A, Raine J, Willenbring J, Williams M, Wolfe A (2008) Mid-Miocene cooling and the extinction of tundra in continental Antarctica. P Natl Acad Sci USA 105:10676–10680

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Livermore R, Nankivell A, Eagles G, Morries P (2005) Paleogene opening of Drake Passage. Earth Planet Sci Lett 236:459–470

    Article  CAS  Google Scholar 

  • Lyle M, Gibbs S, Moore T, Rea D (2007) Late Oligocene initiation of the Antarctic Circumpolar Current: evidence from the South Pacific. Geology 35:691–694

    Article  Google Scholar 

  • Mackensen A (2004) Changing Southern Ocean paleocirculation and effect on global climate. Antarct Sci 16:369–384

    Article  Google Scholar 

  • Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the Notothenioid adaptive radiation. PLoS One 6(4):1–9

    Article  Google Scholar 

  • Near T (2004) Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarct Sci 16:37–44

    Article  Google Scholar 

  • Near T, Cheng C-HC (2008) Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): Inferences from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 47:832–840

    Article  CAS  PubMed  Google Scholar 

  • Near T, Dornburg A, Kuhn K, Eastman J, Pennington J, Patarnello T, Zame L, Fernández DA, Jones C (2012) Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. P Natl Acad Sci USA 109:3434–3439

    Article  CAS  Google Scholar 

  • Nong GT, Najjar RG, Seidov D, Peterson WH (2000) Simulation of ocean temperature change due to the opening of Drake Passage. Geophys Res Lett 27:2689–2692

    Article  Google Scholar 

  • Nybelin O (1947) Antarctic fishes. Scientific results of the Norwegian Antarctic Expeditions 1927–1928 et spp. Nor Vidensk-Akad Oslo Arbok 2(26):1–76

  • Pagani M, Zachos JC, Freeman KH, Tipple B, Bohaty S (2005) Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309:600–603

    Article  CAS  PubMed  Google Scholar 

  • Page T, Linse K (2002) More evidence of speciation and dispersal across the Antarctic Polar Front through molecular systematics of Southern Ocean Limatula (Bivalvia: Limidae). Polar Biol 25:818–826

    Google Scholar 

  • Patarnello T, Bargelloni L, Varotto V, Battaglia B (1996) Krill evolution and the Antarctic Ocean currents: evidence of vicariant speciation as inferred by molecular data. Mar Biol 126:603–608

    Article  Google Scholar 

  • Peck L, Clark M, Clarke A, Cockell C, Convey P, Detrich W III, Fraser K, Johnston I, Methe B, Murray A, Römish K, Rogers A (2005) Genomics: applications to Antarctic ecosystems. Polar Biol 28:351–365

    Article  Google Scholar 

  • Pérez AF, Calvo J, Tresguerres M, Luquet C (2003) Aglomerularism in Harpagifer bispinis: a subantarctic notothenioid fish living at reduced salinity. Polar Biol 26:800–805

    Article  Google Scholar 

  • Pfuhl H, McCave N (2005) Evidence for late Oligocene establishment of the Antarctic Circumpolar Current. Earth Planet Sci Lett 235:715–728

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Poulin E, González-Wevar C, Díaz A, Gérard K, Hüne M (2014) Divergence between Antarctic and South American marine invertebrates: what molecules tell us about Scotia Arc geodynamics and the intensification of the Antarctic Circumpolar Current. Glob Planet Change. doi:10.1016/j.gloplacha.2014.07.017

  • Rabassa J (2008) Late Cenozoic glaciations in Patagonia and Tierra del Fuego. In: Rabassa J (ed) Late Cenozoic of Patagonia and Tierra del Fuego. Developments in Quaternary science. Elsevier, Amsterdam, pp 151–204

    Chapter  Google Scholar 

  • Ronquist F, Huelsenbeck J (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck J, Teslenko M (2011) MrBayes (Bayesian analysis of phylogeny), Version 3.2. http://mrbayes.net

  • Rutshmann S, Matschiner M, Damerau M, Muschick M, Lehmann M, Hanel R, Salzburger W (2011) Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol Ecol 22:4707–4721

    Article  Google Scholar 

  • Salzburger W, Ewing G, Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963

    Article  PubMed  Google Scholar 

  • Scher H, Martin E (2006) Timing and climatic consequences of the opening of Drake Passage. Science 312:428–430

    Article  CAS  PubMed  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Shevenell A, Kennett J, Lea D (2004) Middle Miocene Southern Ocean cooling and Antarctic cryosphere expansion. Science 305:1766–1770

    Article  CAS  PubMed  Google Scholar 

  • Stankovic A, Spalik K, Kamler E, Borsuk P, Weglenski P (2002) Recent origin of sub-Antarctic notothenioids. Polar Biol 25:203–205

    Google Scholar 

  • Strugnell J, Rogers A, Prodohl P, Collins M, Allcock A (2008) The thermohaline expressway: the Southern Ocean as a centre of origin for deep-sea octopuses. Cladistics 24:1–8

    Article  Google Scholar 

  • Thatje S, Hillenbrand C-D, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540

    Article  PubMed  Google Scholar 

  • Thornhill D, Mahon A, Norenburg J, Halanych K (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  CAS  PubMed  Google Scholar 

  • Verducci M, Foresi L, Scott G, Sprovieri M, Lirer F, Pelosi N (2009) The Middle Miocene climatic transition in the Southern Ocean: evidence of paleoclimatic and hydrographic changes at Kerguelen plateau from planktonic foraminifers and stable isotopes. Palaeogeogr Palaeocl 280:371–386

    Article  Google Scholar 

  • Waters J, Fraser C, Hewitt G (2013) Founders takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28(2):78–85

    Article  PubMed  Google Scholar 

  • White M, Burren P (1992) Reproduction and larval growth of Harpagifer antarcticus Nybelin (Pises, Notothenioidei). Antarct Sci 4:421–430

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  CAS  PubMed  Google Scholar 

  • Zachos J, Quinn T, Salamy K (1996) High resolution (104 years) deep-sea foraminiferal stable isotope records of the Eocene–Oligocene climate transition. Paleoceanography 11:251–266

    Article  Google Scholar 

  • Zachos J, Pagani L, Sloan E, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    Article  CAS  PubMed  Google Scholar 

  • Zachos J, Dickens G, Zeebe R (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451:279–283

    Article  CAS  PubMed  Google Scholar 

  • Zhuang X, Cheng C-HC (2010) ND6 gene “Lost” and found: evolution of mitochondrial gene rearrangement in Antarctic Notothenioids. Mol Biol Evol 27(6):1391–1403

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Christina Cheng for constructive comments on the original manuscript. The following Projects supported this study: MSc thesis project INACH M_10–11 and Institute of Ecology and Biodiversity (IEB) PFB-23-2008.

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Authors and Affiliations

  1. Instituto de Ecología y Biodiversidad (IEB), Casilla 653, Santiago, Chile

    Mathias Hüne, Claudio González-Wevar, Elie Poulin & Andrés Mansilla

  2. Laboratorio de Ecología Molecular (LEM), Departamento de Ciencias Ecológicas, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile

    Mathias Hüne, Claudio González-Wevar & Elie Poulin

  3. Departamento de Recursos Naturales, Universidad de Magallanes, Avenida Bulnes 01855, Punta Arenas, Chile

    Mathias Hüne & Andrés Mansilla

  4. Fundación Ictiológica, Pedro de Valdivia 2086/406, Santiago, Chile

    Mathias Hüne

  5. GAIA-Antártica, Universidad de Magallanes, Avenida Bulnes 01890, 621-0427, Punta Arenas, Chile

    Claudio González-Wevar

  6. Centro Austral de Investigaciones Científicas (CADIC-CONICET), Bernardo Houssay 200, Ushuaia, Argentina

    Daniel A. Fernández

  7. Instituto Antártico Argentino, Cerrito 1248, Buenos Aires, Argentina

    Esteban Barrera-Oro

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  1. Mathias Hüne
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Hüne, M., González-Wevar, C., Poulin, E. et al. Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula. Polar Biol 38, 607–617 (2015). https://doi.org/10.1007/s00300-014-1623-6

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