Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-06-09T16:44:58.525Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  28 September 2015

Tshoanelo Miya ,
Ofer Gon ,
Monica Mwale  and
C.-H. Christina Cheng
Tshoanelo Miya*
Affiliation:
South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa Department of Ichthyology and Fisheries, Rhodes University, PO Box 94, Grahamstown 6140, South Africa
Ofer Gon
Affiliation:
South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa
Monica Mwale
Affiliation:
South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa National Zoological Gardens of South Africa, PO Box 754, Pretoria 0001, South Africa
C.-H. Christina Cheng
Affiliation:
Department of Animal Biology, University of Illinois, Urbana-Champaign, 515 Morrill Hall, 505 South Goodwin, Urbana, IL 61801, USA
*
t.miya@saiab.ac.za
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

antifreeze glycoprotein (AFGP) traitevolutionary originnon-freezing waternotothenioids
Type
Biological Sciences
Information
Antarctic Science , Volume 28 , Supplement 1 , February 2016 , pp. 17 - 28
Check for updates
Copyright
© Antarctic Science Ltd 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bilyk, K.T. & DeVries, A.L. 2010. Freezing avoidance of the Antarctic icefishes (Channichthyidae) across thermal gradients on the Southern Ocean. Polar Biology, 33, 203–213.CrossRefGoogle Scholar
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, 3811–3816.CrossRefGoogle ScholarPubMed
Cheng, C-H.C. & Detrich III, H.W. 2007. Molecular ecophysiology of Antarctic notothenioid fishes. Philosophical Transactions of the Royal Society, B362, 2215–2232.CrossRefGoogle Scholar
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, 1897–1908.Google Scholar
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, 14 583–14 588.Google Scholar
Darriba, D., Taboada, G.L., Doalla, R. & Posada, D. 2012. jModelTest2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.Google Scholar
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, 2–9.Google Scholar
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, 49–58.CrossRefGoogle ScholarPubMed
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 1152–1155.Google Scholar
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, 293–303.Google Scholar
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, 155–201.Google Scholar
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, 439–458.Google Scholar
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 279–331.Google Scholar
Eastman, J.T. 2005. The nature of the diversity of Antarctic fishes. Polar Biology, 28, 93–107.Google Scholar
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, 53–56.Google Scholar
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, 3023–3032.Google Scholar
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, 307–321.Google Scholar
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, 27 637–27 653.Google Scholar
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, 9265–9269.Google Scholar
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.Google Scholar
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].Google Scholar
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, 290–300.Google Scholar
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, 1993–2009.CrossRefGoogle Scholar
Kennett, J.P. 1982. Marine geology. Englewood Cliffs, NJ: Prentice-Hall, 813 pp.Google Scholar
Knox, G.A. 2007. Biology of the Southern Ocean, 2nd edition. Boca Raton, FL: CRC Press, 621 pp.Google Scholar
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, 420–432.Google Scholar
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, 416–449.Google Scholar
Matschiner, M., Hanel, R. & Salburger, W. 2009. Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons . Molecular Ecology, 18, 2574–2587.Google Scholar
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, 367–373.Google Scholar
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, 832–840.Google Scholar
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, 3434–3439.Google Scholar
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, 194–201.Google Scholar
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, 507–527.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.Google Scholar
Swofford, D.L. 2003. PAUP* v4: phlyogenetic analysis using parsimony (and other methods). Sunderland, MA: Sinauer Associates.Google Scholar
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, 2731–2739.Google Scholar
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, 47–59.Google Scholar
Supplementary material: PDF

Miya supplementary material

Table S1 and Figure S1

Download Miya supplementary material(PDF)
PDF 604 KB