Skip to main content
×
×
Home

Multiple independent reduction or loss of antifreeze trait in low Antarctic and sub-Antarctic notothenioid fishes

  • Tshoanelo Miya (a1) (a2), Ofer Gon (a1), Monica Mwale (a1) (a3) and C.-H. Christina Cheng (a4)
Abstract

Antifreeze glycoprotein (AFGP) in Antarctic notothenioids presumably evolved once at the base of the notothenioid radiation in the Southern Ocean. Some species closely related to the endemic Antarctic notothenioids occur in non-freezing sub-Antarctic waters where antifreeze protection is unnecessary. We examined the antifreeze trait (phenotype and genotype) of these sub-Antarctic species to help infer their evolutionary history and origin. The status of the AFGP genotype (AFGP coding sequences in DNA) and/or phenotype (serum thermal hysteresis) varies widely, from being undetectable in Dissostichus eleginoides and Patagonotothen species from the Falkland Islands, minimal in Marion Island Paranotothenia magellanica and Lepidonotothen squamifrons from the South Sandwich and Bouvet islands, to considerable genotype in the Falkland Islands Champsocephalus esox and Marion Island Harpagifer georgianus. All low Antarctic notothenioid species examined show substantial AFGP trait. Mapping of the AFGP trait status onto ND2 phylogenetic trees of a large sampling of notothenioids revealed that AFGP trait reduction or loss occurred at least three independent times in different lineages.

Copyright
Corresponding author
t.miya@saiab.ac.za
References
Hide All
Bilyk, K.T. & DeVries, A.L. 2010. Freezing avoidance of the Antarctic icefishes (Channichthyidae) across thermal gradients on the Southern Ocean. Polar Biology, 33, 203213.
Chen, L.B., DeVries, A.L. & Cheng, C.-H.C. 1997. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proceedings of the National Academy of Sciences of the United States of America, 94, 38113816.
Cheng, C-H.C. & Detrich III, H.W. 2007. Molecular ecophysiology of Antarctic notothenioid fishes. Philosophical Transactions of the Royal Society, B362, 22152232.
Cheng, C-H.C., Chen, L.B., Near, T.J. & Jin, Y.M. 2003. Functional antifreeze glycoprotein genes in temperate-water New Zealand Notothenioid fish infer an Antarctic origin. Molecular Biology and Evolution, 20, 18971908.
Cziko, P.A., DeVries, A.L., Evans, C.W. & Cheng, C-H.C. 2014. Antifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warming. Proceedings of the National Academy of Sciences of the United States of America, 111, 14 58314 588.
Darriba, D., Taboada, G.L., Doalla, R. & Posada, D. 2012. jModelTest2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
De Broyer, C. & Koubbi, P. 2014. The biogeography of the Southern Ocean. In De Broyer, C., Koubbi, P., Griffiths, H.J., et al., eds. Biogeographic atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research, 29.
Dettai, A., Berkani, M., Lautredou, A.-C., Couloux, A., Lecointre, G., Ozouf-Costaz, C. & Gallut, C. 2012. Tracking the elusive monophyly of nototheniid fishes (Teleostei) with multiple mitochondrial and nuclear markers. Marine Genomics, 8, 4958.
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 11521155.
DeVries, A.L. 1986. Glycopeptide and peptide antifreeze: interaction with ice. In Colowick, S.P. & Kaplan, N.O., eds. Methods enzymol. New York, NY: Academic Press, 293303.
DeVries, A.L. & Cheng, C.-H.C. 2005. Antifreeze proteins and organismal freezing avoidance in polar fishes. In Farrell, A.P. & Steffensen, J.F., eds. Fish physiology, Vol 22. San Diego, CA: Academic Press, 155201.
DeVries, A.L. & Lin, Y. 1977. The role of glycoprotein antifreezes in the survival of Antarctic fishes. In Llano, G.A., ed. Adaptation within Antarctic ecosystems. Proceedings of the Third Symposium on Antarctic Biology. Houston, TX: Gulf Publishing, 439458.
DeWitt, H.H., Heemstra, P.C. & Gon, O. 1990. Nototheniidae. In Gon, O. & Heemstra, P.C., eds. Fishes of the Southern Ocean. Grahamstown: J.L.B., Smith Institute of Ichthyology 279331.
Eastman, J.T. 2005. The nature of the diversity of Antarctic fishes. Polar Biology, 28, 93107.
Gon, O., Hendry, D.A. & Mostert, D. 1994. Glycoprotein antifreeze in Notothenia coriiceps (Pisces: Nototheniidae) from the sub-Antarctic Marion Island. South African Journal of Antarctic Research, 24, 5356.
Gordon, A.L., Molinelli, E. & Baker, T. 1978. Large-scale relative dynamic topography of the Southern Ocean. Journal of Geophysical Research - Oceans and Atmospheres, 83, 30233032.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307321.
Haine, T.W.N., Watson, A.J., Liddicoat, M.I. & Dickson, R.R. 1998. The flow of Antarctic Bottom Water to the southwest Indian Ocean estimated using CFCs. Journal of Geophysical Research - Oceans, 103, 27 63727 653.
Hsiao, K.C., Cheng, C.-H.C., Fernandes, I.E., Detrich, H.W. & DeVries, A.L. 1990. An antifreeze glycopeptide gene from the Antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proceedings of the Natural Academy of Sciences of the United State of America, 87, 92659269.
Hüne, M., González-Wevar, C., Poulin, E., Mansilla, A., Fernandez, D.A. & Barrera-Oro, E. 2014. Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula. Polar Biology, 10.1007/s00300-014-1623-6.
Jin, Y. 2003. Freezing avoidance of Antarctic fishes: the role of a novel antifreeze potentiating protein and the antifreeze glycoproteins. PhD thesis, University of Illinois, Urbana-Champaign, 202 pp. [Unpublished].
Jin, Y. & DeVries, A.L. 2006. Antifreeze glycoprotein levels in Antarctic notothenioid fishes inhabiting different thermal environment and the effects of warm acclimation. Comparative Biochemistry and Physiology, 144B, 290300.
Kemp, A.E.S., Grigorov, I., Pearce, R.B. & Garabato, A.C.N. 2010. Migration of the Antarctic Polar Front through the mid-Pleistocene transition: evidence and climatic implications. Quaternary Science Reviews, 29, 19932009.
Kennett, J.P. 1982. Marine geology. Englewood Cliffs, NJ: Prentice-Hall, 813 pp.
Knox, G.A. 2007. Biology of the Southern Ocean, 2nd edition. Boca Raton, FL: CRC Press, 621 pp.
Kocher, T.D., Conroy, J.A., McKaye, K.R., Stauffer, J.R. & Lockwood, S.F. 1995. Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Molecular Phylogenetics and Evolution, 4, 420432.
Loeb, V.J., Kellermann, A.K., Koubbi, P., North, A.W. & White, M.G. 1993. Antarctic larval fish assemblages – a review. Bulletin of Marine Science, 53, 416449.
Matschiner, M., Hanel, R. & Salburger, W. 2009. Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons . Molecular Ecology, 18, 25742587.
Miya, T., Gon, O., Mwale, M. & Cheng, C.-H.C. 2014. The effect of habitat temperature on serum antifreeze glycoprotein (AFGP) activity in Notothenia rossii (Pisces: Nototheniidae) in the Southern Ocean. Polar Biology, 37, 367373.
Near, T.J. & Cheng, C.-H.C. 2008. Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): inference from mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution, 47, 832840.
Near, T.J., Dornburg, A., Kuhn, K.L., Eastman, J.T., Pennington, J.N., Patarnello, T., Zane, L., Fenandez, D.A. & Jones, C.D. 2012. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proceedings of the National Academy of Science of the United States of America, 109, 34343439.
Nicodemus-Johnson, J., Silic, S., Ghigliotti, L., Pisano, E. & Cheng, C.-H.C. 2011. Assembly of the antifreeze glycoprotein/trypsinogen-like protease genomic locus in the Antarctic toothfish Dissostichus mawsoni (Norman). Genomics, 98, 194201.
Rhein, M., Stramma, L. & Krahmann, G. 1998. The spreading of Antarctic bottom water in the tropical Atlantic. Deep-Sea Research I - Oceanographic Research Papers, 45, 507527.
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 15721574.
Swofford, D.L. 2003. PAUP* v4: phlyogenetic analysis using parsimony (and other methods). Sunderland, MA: Sinauer Associates.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution, 28, 27312739.
Wöhrmann, A.P.A. 1996. Antifreeze glycopeptides and peptides in Antarctic fish species from the Weddell Sea and the Lazarev Sea. Marine Ecology Progress Series, 130, 4759.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Antarctic Science
  • ISSN: 0954-1020
  • EISSN: 1365-2079
  • URL: /core/journals/antarctic-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
PDF
Supplementary materials

Miya supplementary material
Table S1 and Figure S1

 PDF (604 KB)
604 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed