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The Adaptive Radiation of Notothenioid Fishes in the Waters of Antarctica

  • Michael Matschiner
  • Marco Colombo
  • Malte Damerau
  • Santiago Ceballos
  • Reinhold Hanel
  • Walter Salzburger
Chapter

Abstract

Fishes of the perciform suborder Notothenioidei, which dominate the ichthyofauna in the freezing waters surrounding the Antarctic continent, represent one of the prime examples of adaptive radiation in a marine environment. Driven by unique adaptations, such as antifreeze glycoproteins that lower their internal freezing point, notothenioids have not only managed to adapt to sub-zero temperatures and the presence of sea ice, but also diversified into over 130 species. We here review the current knowledge about the most prominent notothenioid characteristics, how these evolved during the evolutionary history of the suborder, how they compare between Antarctic and non-Antarctic groups of notothenioids, and how they could relate to speciation processes.

Keywords

Adaptive Radiation Antarctic Circumpolar Current Antarctic Water Diversification Rate Species Flock 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank the editors and Joseph Eastman for valuable comments on the manuscript. The authors of this book chapter have been supported by funding from the Swiss National Science Foundation (SNF grants PBBSP3-138680 to MM and CRSII3-136293 to WS), the European Research Council (Starting Grant “INTERGENADAPT” to WS), the Volkswagen Foundation (grant I/83 548 to MM), and the German Research Foundation (grant HA 4328/4 to RH).

References

  1. Agostini C, Papetti C, Patarnello T et al (2013) Putative selected markers in the Chionodraco genus detected by interspecific outlier tests. Polar Biol 36:1509–1518Google Scholar
  2. Albertson RC, Yan Y-L, Titus TA et al (2010) Molecular pedomorphism underlies craniofacial skeletal evolution in Antarctic notothenioid fishes. BMC Evol Biol 10:4PubMedCentralPubMedGoogle Scholar
  3. Anderson JB (1999) Antarctic marine geology. Cambridge University Press, CambridgeGoogle Scholar
  4. Balushkin AV (1992) Classification, phylogenetic relationships, and origins of the families of the suborder Notothenioidei (Perciformes). J Ichthyol 32:90–110Google Scholar
  5. Balushkin AV (1994) Fossil notothenioid, and not gadiform, fish Proeleginops grandeastmanorum gen. sp. nov. (Perciformes, Notothenioidei, Eleginopidae) from the late Eocene found in Seymour Island (Antarctica). Voprosy Ikhtiologii 34:298–307Google Scholar
  6. Balushkin AV (2000) Morphology, classification, and evolution of notothenioid fishes of the Southern Ocean (Notothenioidei, Perciformes). J Ichthyol 40:S74–S109Google Scholar
  7. Balushkin AV (2012) Volodichthys gen. nov. new species of the primitive snailfish (Liparidae: Scorpaeniformes) of the southern hemishpere. Description of new species V. Solovjevae sp. nov. (Cooperation Sea, the Antarctic). J Ichthyol 52:1–10Google Scholar
  8. Bargelloni L, Marcato S, Zane L, Patarnello T (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst Biol 49:114–129PubMedGoogle Scholar
  9. Barker PF, Filippelli GM, Florindo F, Martin EE, Scher HD (2007) Onset and role of the Antarctic circumpolar current. Deep Sea Res Pt II 54:2388–2398Google Scholar
  10. Barnes DKA, Conlan KE (2007) Disturbance, colonization and development of Antarctic benthic communities. Philos Trans R Soc B 362:11–38Google Scholar
  11. Barnes DKA, Hodgson DA, Convey P, Allen CS, Clarke A (2006) Incursion and excursion of Antarctic biota: past, present and future. Global Ecol Biogeogr 15:121–142Google Scholar
  12. Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256Google Scholar
  13. Betancur-R R, Broughton RE, Wiley EO et al (2013) The Tree of Life and a new classification of bony fishes. PLoS Curr 5:18Google Scholar
  14. Bilyk KT, DeVries AL (2010) Freezing avoidance of the Antarctic icefishes (Channichthyidae) across thermal gradients in the Southern Ocean. Polar Biol 33:203–213Google Scholar
  15. Bilyk KT, DeVries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A 158:382–390Google Scholar
  16. Bilyk KT, Evans CW, DeVries AL (2012) Heat hardening in Antarctic notothenioid fishes. Polar Biol 35:1447–1451Google Scholar
  17. Carvalho GR, Warren M (1991) Genetic population structure of the mackerel icefish, Champsocephalus gunnari, in Antarctic waters. Document WG-FSA-91/22. CCAMLR working paperGoogle Scholar
  18. Chen L, DeVries AL, Cheng C-HC (1997a) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 94:3811–3816PubMedCentralPubMedGoogle Scholar
  19. Chen L, DeVries AL, Cheng C-HC (1997b) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci U S A 94:3817–3822PubMedCentralPubMedGoogle Scholar
  20. Cheng C-HC, Detrich HW III (2007) Molecular ecophysiology of Antarctic notothenioid fishes. Philos Trans R Soc B 362:2215–2232Google Scholar
  21. Cheng C-HC, DeVries AL (1989) Structures of antifreeze peptides from the Antarctic eel pout, Austrolycicthys brachycephalus. Biochim Biophys Acta 997:55–64PubMedGoogle Scholar
  22. Cheng C-HC, Chen L, Near TJ, Jin Y (2003) Functional antifreeze glycoprotein genes in temperate-water New Zealand nototheniid fish infer an Antarctic evolutionary origin. Mol Biol Evol 20:1897–1908PubMedGoogle Scholar
  23. Cheng C-HC, Cziko PA, Evans CW (2006) Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc Natl Acad Sci U S A 103:10491–10496PubMedCentralPubMedGoogle Scholar
  24. Claeson KM, Eastman JT, MacPhee RDE (2012) Definitive specimens of Merlucciidae (Gadiformes) from the Eocene James Ross Basin of Isla Marambio (Seymour Island), Antarctic Peninsula. Antarct Sci 24:467–472Google Scholar
  25. Clark MS, Fraser KPP, Burns G, Peck LS (2008) The HSP70 heat shock response in the Antarctic fish Harpagifer antarcticus. Polar Biol 31:171–180Google Scholar
  26. Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Physiol B 90:461–473Google Scholar
  27. Cocca E, Ratnayake-Lecamwasam M, Parker SK et al (1995) Genomic remnants of alpha-globin genes in the hemoglobinless Antarctic icefishes. Proc Natl Acad Sci U S A 92:1817–1821PubMedCentralPubMedGoogle Scholar
  28. Coppes Petricorena ZL, Somero GN (2007) Biochemical adaptations of notothenioid fishes: comparisons between cold temperate South American and New Zealand species and Antarctic species. Comp Biochem Physiol A 147:799–807Google Scholar
  29. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466PubMedGoogle Scholar
  30. Cziko PA, Evans CW, Cheng C-HC, DeVries AL (2006) Freezing resistance of antifreeze-deficient larval Antarctic fish. J Exp Biol 209:407–420PubMedGoogle Scholar
  31. 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, Antarctica. Polar Biol 35:1073–1086Google Scholar
  32. Damerau M, Matschiner M, Salzburger W, Hanel R (2014) Population divergences despite long pelagic larval stages: lessons from crocodile icefishes (Channichthyidae). Mol Ecol 23:284–299Google Scholar
  33. DeConto RM, Pollard D (2003) Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2. Nature 421:245–249PubMedGoogle Scholar
  34. Derome N, Chen W-J, Dettaï A, Bonillo CÉ, Lecointre G (2002) Phylogeny of Antarctic dragonfishes (Bathydraconidae, Notothenioidei, Teleostei) and related families based on their anatomy and two mitochondrial genes. Mol Phylogenet Evol 24:139–152PubMedGoogle Scholar
  35. Dettaï A, Lecointre G (2004) In search of notothenioid (Teleostei) relatives. Antarct Sci 16:71–85Google Scholar
  36. Dettai A, Berkani M, Lautrédou A-C et al (2012) Tracking the elusive monophyly of nototheniid fishes (Teleostei) with multiple mitochondrial and nuclear markers. Mar Genomics 8:49–58PubMedGoogle Scholar
  37. DeVries AL, Cheng CH (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. In: Farrell AP, Steffensen JF (eds) Fish physiology, vol 22. Academic Press, San Diego, CA, pp 155–201Google Scholar
  38. DeVries AL, Eastman JT (1978) Lipid sacs as a buoyancy adaptation in an Antarctic fish. Nature 271:352–353Google Scholar
  39. di Prisco G, Cocca E, Parker SK, Detrich HW III (2002) Tracking the evolutionary loss of hemoglobin expression by the white-blooded Antarctic icefishes. Gene 295:185–191PubMedGoogle Scholar
  40. 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 430–436Google Scholar
  41. Eastman JT (1993) Antarctic fish biology: evolution in a unique environment. Academic Press, San Diego, CAGoogle Scholar
  42. Eastman JT (2000) Antarctic notothenioid fishes as subjects for research in evolutionary biology. Antarct Sci 12:276–287Google Scholar
  43. Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107Google Scholar
  44. Eastman JT, Clarke A (1998) A comparison of adaptive radiations of Antarctic fish with those of nonAntarctic fish. In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica. A biological overview. Springer, Milano, pp 3–26Google Scholar
  45. Eastman JT, Eakin RR (2000) An updated species list for notothenioid fish (Perciformes; Notothenioidei), with comments on Antarctic species. Arch Fish Mar Res 48:11–20Google Scholar
  46. Eastman JT, Grande L (1991) Late Eocene gadiform (Teleostei) skull from Seymour Island, Antarctic Peninsula. Antarct Sci 3:87–95Google Scholar
  47. Eastman JT, McCune AR (2000) Fishes on the Antarctic continental shelf: evolution of a marine species flock? J Fish Biol 57:84–102Google Scholar
  48. Evans JD, Page LM (2003) Distribution and relative size of the swim bladder in Percina, with comparisons to Etheostoma, Crystallaria, and Ammocrypta (Teleostei: Percidae). Environ Biol Fish 66:61–65Google Scholar
  49. Evans CW, Gubala V, Nooney R et al (2011) How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins. Antarct Sci 23:57–64Google Scholar
  50. Evans CW, Hellman L, Middleditch M et al (2012) Synthesis and recycling of antifreeze glycoproteins in polar fishes. Antarct Sci 24:259–268Google Scholar
  51. Fernández DA, Ceballos SG, Malanga G, Boy CC, Vanella FA (2012) Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae). Polar Biol 35:99–106Google Scholar
  52. Fletcher GL, Hew C-L, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390PubMedGoogle Scholar
  53. Foster TD (1984) The marine environment. In: Laws RM (ed) Antarctic ecology, vol 2. Academic Press, London, pp 345–371Google Scholar
  54. Gavrilets S, Losos JB (2009) Adaptive radiation: contrasting theory with data. Science 323:732–737PubMedGoogle Scholar
  55. Gavrilets S, Vose A (2005) Dynamic patterns of adaptive radiation. Proc Natl Acad Sci U S A 102:18040–18045PubMedCentralPubMedGoogle Scholar
  56. 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. Quaternary Sci Rev 24:869–896Google Scholar
  57. Gon O, Heemstra PC (1990) Fishes of the Southern Ocean. J.L.B. Smith Institute of Ichthyology, GrahamstownGoogle Scholar
  58. González-Wevar CA, Nakano T, Cañete JI, Poulin E (2011) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Mol Ecol 20:1936–1951PubMedGoogle Scholar
  59. Gordon AL (1971) Oceanography of Antarctic waters. In: Reid JL (ed) Antarctic oceanology I. American Geophysical Union, Washington, DC, pp 169–203Google Scholar
  60. Graham LA, Lougheed SC, Ewart KV, Davies PL (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS One 3:e2616PubMedCentralPubMedGoogle Scholar
  61. Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580PubMedCentralPubMedGoogle Scholar
  62. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276Google Scholar
  63. Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae). J Exp Biol 203:2331–2339PubMedGoogle Scholar
  64. Hofmann GE, Lund SG, Place SP, Whitmer AC (2005) Some like it hot, some like it cold: the heat shock response is found in New Zealand but not Antarctic notothenioid fishes. J Exp Mar Biol Ecol 316:79–89Google Scholar
  65. Hsiao K-C, Cheng C-HC, Fernandes IE, Detrich HW III, DeVries AL (1990) An antifreeze glycopeptide gene from the antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proc Natl Acad Sci U S A 87:9265–9269PubMedCentralPubMedGoogle Scholar
  66. Ingólfsson Ó (2004) Quaternary glacial and climate history of Antarctica. Dev Quaternary Sci 2C:3–44Google Scholar
  67. Ivany LC, Lohmann KC, Hasiuk F et al (2008) Eocene climate record of a high southern latitude continental shelf: Seymour Island, Antarctica. Geol Soc Am Bull 120:659–678Google Scholar
  68. Janko K, Lecointre G, DeVries AL et al (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 7:220PubMedCentralPubMedGoogle Scholar
  69. Janko K, Marshall C, Musilová Z et al (2011) Multilocus analyses of an Antarctic fish species flock (Teleostei, Notothenioidei, Trematominae): phylogenetic approach and test of the early-radiation event. Mol Phylogenet Evol 60:305–316PubMedGoogle Scholar
  70. Johnston IA, Fernández DA, Calvo J et al (2003) Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective. J Exp Biol 206:2595–2609PubMedGoogle Scholar
  71. Kennett JP (1982) Marine geology. Prentice Hall, Englewood Cliffs, NJGoogle Scholar
  72. Klingenberg CP, Ekau W (1996) A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biol J Linn Soc 59:143–177Google Scholar
  73. Koblmüller S, Egger B, Sturmbauer C, Sefc KM (2010) Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Mol Phylogenet Evol 55:318–334PubMedGoogle Scholar
  74. La Mesa M, Ashford J (2008) Age and early life history of juvenile Scotia Sea icefish, Chaenocephalus aceratus, from Elephant and the South Shetland Islands. Polar Biol 31:221–228Google Scholar
  75. 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 27:321–338Google Scholar
  76. Last PR, Balushkin AV, Hutchins JB (2002) Halaphritis platycephala (Notothenioidei: Bovichtidae): a new genus and species of temperate icefish from Southeastern Australia. Copeia 2002:433–440Google Scholar
  77. Lautrédou A-C, Hinsinger DD, Gallut C et al (2012) Phylogenetic footprints of an Antarctic radiation: the Trematominae (Notothenioidei, Teleostei). Mol Phylogenet Evol 65:87–101PubMedGoogle Scholar
  78. Lautrédou A-C, Motomura H, Gallut C et al (2013) New nuclear markers and exploration of the relationships among Serraniformes (Acanthomorpha, Teleostei): the importance of working at multiple scales. Mol Phylogenet Evol 67:140–155PubMedGoogle Scholar
  79. Lewis DB (1976) Studies of the biology of the lesser weever. J Fish Biol 8:127–138Google Scholar
  80. Loeb VJ, Kellermann AK, Koubbi P, North AW, White MG (1993) Antarctic larval fish assemblages: a review. Bull Mar Sci 53:416–449Google Scholar
  81. Long DJ (1992) Sharks from the La Meseta Formation (Eocene), Seymour Island, Antarctic Peninsula. J Vertebr Paleontol 12:11–32Google Scholar
  82. Matallanas J (2008) Description of Gosztonyia antarctica, a new genus and species of Zoarcidae (Teleostei: Perciformes) from the Antarctic Ocean. Polar Biol 32:15–19Google Scholar
  83. Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587PubMedGoogle Scholar
  84. Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the notothenioid adaptive radiation. PLoS One 6:e18911PubMedCentralPubMedGoogle Scholar
  85. Muschick M, Indermaur A, Salzburger W (2012) Convergent evolution within an adaptive radiation of cichlid fishes. Curr Biol 22:2362–2368PubMedGoogle Scholar
  86. Naish TR, Woolfe KJ, Barrett PJ et al (2001) Orbitally induced oscillations in the East Antarctic ice sheet at the Oligocene/Miocene boundary. Nature 413:719–723PubMedGoogle Scholar
  87. Near TJ (2004) Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarct Sci 16:37–44Google Scholar
  88. Near TJ, Cheng C-HC (2008) Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): inferences from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 47:1–9Google Scholar
  89. Near TJ, Pesavento JJ, Cheng C-HC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol Phylogenet Evol 32:881–891PubMedGoogle Scholar
  90. Near TJ, Parker SK, Detrich HW III (2006) A genomic fossil reveals key steps in hemoglobin loss by the Antarctic icefishes. Mol Biol Evol 23:2008–2016PubMedGoogle Scholar
  91. Near TJ, Dornburg A, Kuhn KL et al (2012) Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc Natl Acad Sci U S A 109:3434–3439PubMedCentralPubMedGoogle Scholar
  92. Nelson JS (2006) Fishes of the world. John Wiley, Hoboken, NJGoogle Scholar
  93. Nong GT, Najjar RG, Seidov D, Peterson WH (2000) Simulation of ocean temperature change due to the opening of Drake Passage. Geophys Res Lett 27:2689–2692Google Scholar
  94. Nosil P (2012) Ecological speciation. Oxford University Press, New York, NYGoogle Scholar
  95. Ojeda FP, Labra FA, Muñoz AA (2000) Biogeographic patterns of Chilean littoral fishes. Revista Chilena de Historia Natural 73:625–641Google Scholar
  96. Olney MP, Bohaty SM, Harwood DM (2009) Creania lacyae gen. nov et sp. nov and Synedropsis cheethamii sp. nov., fossil indicators of Antarctic sea ice? Diatom Res 24:357–375Google Scholar
  97. Pequeño RG (2000) Peces del crucero Cimar-Fiordo 3, a los canales del sur de Magallanes (ca. 55°S), Chile. Ciencia y Tecnología del Mar 23:83–94Google Scholar
  98. Petit JR, Jouzel J, Barkov NI et al (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399:429–436Google Scholar
  99. Place SP, Hofmann GE (2005) Constitutive expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antarctic fish. Polar Biol 28:261–267Google Scholar
  100. Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes. Am J Physiol-Reg I 287:R429–R436Google Scholar
  101. Præbel K, Hunt B, Hunt LH, DeVries AL (2009) The presence and quantification of splenic ice in the McMurdo Sound Notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902). Comp Biochem Physiol A 154:564–569Google Scholar
  102. Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philos Trans R Soc B 362:2191–2214Google Scholar
  103. Rogers AD, Morley S, Fitzcharles E, Jarvis K, Belchier M (2006) Genetic structure of Patagonian toothfish (Dissostichus eleginoides) populations on the Patagonian Shelf and Atlantic and western Indian Ocean Sectors of the Southern Ocean. Mar Biol 149:915–924Google Scholar
  104. Rutschmann S, Matschiner M, Damerau M et al (2011) Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol Ecol 20:4707–4721PubMedGoogle Scholar
  105. Ruud JT (1954) Vertebrates without erythrocytes and blood pigment. Nature 173:848–850PubMedGoogle Scholar
  106. Salzburger W, Meyer A (2004) The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 91:277–290PubMedGoogle Scholar
  107. Salzburger W, Van Bocxlaer B, Cohen AS (2014) Ecology and evolution of the African Great Lakes and their faunas. Annu Rev Ecol Evol Syst 45:519–545Google Scholar
  108. Scher HD, Martin EE (2006) Timing and climatic consequences of the opening of Drake Passage. Science 428:428–430Google Scholar
  109. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New York, NYGoogle Scholar
  110. Shaw PW, Arkhipkin AI, 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 13:3293–3303PubMedGoogle Scholar
  111. Shevenell AE, Kennett JP, Lea DW (2004) Middle Miocene Southern Ocean cooling and Antarctic cryosphere expansion. Science 305:1766–1770PubMedGoogle Scholar
  112. Sidell BD, O’Brien K (2006) When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes. J Exp Biol 209:1791–1802PubMedGoogle Scholar
  113. Smith P, Gaffney PM (2000) Toothfish stock structure revealed with DNA methods. Water Atmos 8:17–18Google Scholar
  114. Smith PJ, Gaffney PM (2005) Low genetic diversity in the Antarctic toothfish (Dissostichus mawsoni) observed with mitochondrial and intron DNA markers. CCAMLR Sci 12:43–51Google Scholar
  115. Stankovic A, Spalik K, Kamler E, Borsuk P, Weglenski P (2002) Recent origin of sub-Antarctic notothenioids. Polar Biol 25:203–205Google Scholar
  116. Stein DL (2012) Snailfishes (Family Liparidae) of the Ross Sea, Antarctica, and closely adjacent waters. Zootaxa 3285:1–120Google Scholar
  117. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109PubMedGoogle Scholar
  118. Team CRS (2000) Studies from the Cape Roberts project, Ross Sea, Antarctica. Initial report on CRP-3. Terra Antarctica 7:1–209Google Scholar
  119. Thatje S, Hillenbrand C-D, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540PubMedGoogle Scholar
  120. Tomczak M, Godfrey JS (2003) Regional oceanography: an introduction. Daya Publishing House, DelhiGoogle Scholar
  121. Volckaert FAM, Rock J, Putte AP (2012) Connectivity and molecular ecology of Antarctic fishes. In: di Prisco G, Verde C (eds) Adaptation and evolution in marine environments, vol 1. Springer, Berlin, pp 75–96Google Scholar
  122. von der Heyden BP, Roychoudhury AN, Mtshali TN, Tyliszczak T, Myneni SCB (2012) Chemically and geographically distinct solid-phase iron pools in the Southern Ocean. Science 338:1199–1201PubMedGoogle Scholar
  123. Wilson LAB, Colombo M, Hanel R, Salzburger W, Sánchez-Villagra MR (2013) Ecomorphological disparity in an adaptive radiation: opercular bone shape and stable isotopes in Antarctic icefishes. Ecol Evol 3:3166–3182PubMedCentralPubMedGoogle Scholar
  124. Yoder JB, Clancey E, Des Roches S et al (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23:1581–1596PubMedGoogle Scholar
  125. Zachos JC, Quinn TM, Salamy KA (1996) High resolution (104 years) deep-sea foraminiferal stable isotope records of the Eocene-Oligocene climate transition. Paleoceanography 11:251–266Google Scholar
  126. Zane L, Bargelloni L, Bortolotto E et al (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:4499–4511PubMedGoogle Scholar
  127. Zhuang X (2013) Creating sense from non-sense DNA: de novo genesis and evolutionary history of antifreeze glycoprotein gene in northern cod fishes (Gadidae). Dissertation, School of Integrative Biology, University of Illinois at Urbana-ChampaignGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Michael Matschiner
    • 1
    • 2
  • Marco Colombo
    • 1
  • Malte Damerau
    • 3
  • Santiago Ceballos
    • 1
    • 4
  • Reinhold Hanel
    • 3
  • Walter Salzburger
    • 1
    • 2
  1. 1.Zoological InstituteUniversity of BaselBaselSwitzerland
  2. 2.Centre for Ecological and Evolutionary Synthesis (CEES), Department of BiosciencesUniversity of OsloOsloNorway
  3. 3.Thünen Institute of Fisheries EcologyHamburgGermany
  4. 4.Centro Austral de Investigaciones Científicas (CADIC)UshuaiaArgentina

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