CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Invertebrate Systematics   
Invertebrate Systematics
Journal Banner
  Systematics, Phylogeny and Biogeography
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
Current Issue
Just Accepted
All Issues
Special Issues
Virtual Issues
Sample Issue
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow Supplementary Series
blank image
All volumes of the Australian Journal of Zoology Supplementary Series are online.

 

Article << Previous     |     Next >>   Contents Vol 26(6)

Antarctic Tardigrada: a first step in understanding molecular operational taxonomic units (MOTUs) and biogeography of cryptic meiofauna

Paul Czechowski A B C I , Chester J. Sands C I , Byron J. Adams D , Cyrille A. D’Haese E , John A. E. Gibson F , Sandra J. McInnes C and Mark I. Stevens B G H I

A University of Leipzig, Molecular Evolution and Animal Systematics, Talstrasse 33, 04103 Leipzig, Germany.
B School of Earth and Environmental Sciences, University of Adelaide, SA 5005, Australia.
C British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, UK.
D Department of Biology, Brigham Young University, Provo, UT 84602-5181, USA.
E UMR 7205 CNRS, Origine, Structure et Evolution de la Biodiversite, Departement Systematique et Evolution, Museum national d’Histoire naturelle, CP50 – Entomologie, 75231 Paris cedex 05, France.
F Institute of Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tas. 7001, Australia.
G South Australian Museum, GPO Box 234, Adelaide, SA 5000, Australia.
H Corresponding author: Email: mark.stevens@samuseum.sa.gov.au
I These authors contributed equally

Invertebrate Systematics 26(6) 526-538 http://dx.doi.org/10.1071/IS12034
Submitted: 30 April 2012  Accepted: 4 October 2012   Published: 19 December 2012


 
PDF (1.2 MB) $40
 Supplementary Material
 Export Citation
 Print
  
Abstract

Recent studies have suggested that some resident Antarctic biota are of ancient origin and may have been isolated for millions of years. The phylum Tardigrada, which is part of the Antarctic terrestrial meiofauna, is of particular interest due to an impressive array of biochemical abilities to withstand harsh environmental conditions. Tardigrades are one of the few widespread Antarctic terrestrial animals that have the potential to be used as a model for evolution and biogeography on the Antarctic continent. We isolated 126 individual tardigrades from four geographically isolated soil samples from two remote nunataks in the Sør Rondane Mountains, Dronning Maud Land, Antarctica. We examined genetic variation among individuals utilising three gene regions: cytochrome c oxidase subunit I gene (COI), 18S rDNA (18S), and the wingless (Wg) gene. Comparison of sequences from worldwide and Antarctic tardigrades indicated long-term survival and isolation over glacially dominated periods in ice-free habitats in the Sør Rondane Mountains.



References

Adams, B. J., Bardgett, R. D., Ayres, E., Wall, D. H., Aislabie, J., Bamforth, S., Bargagli, R., Cary, C., Cavacini, P., Connell, L., Convey, P., Fell, J. W., Frati, F., Hogg, I. D., Newsham, K. K., O’Donnell, A., Russell, N., Seppelt, R. D., and Stevens, M. I. (2006). Diversity and distribution of Victoria Land biota. Soil Biology & Biochemistry 38, 3003–3018.
CrossRef | CAS |

Adams, B. J., Wall, D. H., Gozel, U., Dillman, A. R., Chaston, J. M., and Hogg, I. D. (2007). The southernmost worm, Scottnema lindsayae (Nematoda): diversity, dispersal and ecological stability. Polar Biology 30, 809–815.
CrossRef |

Altmaier, M., Herpers, U., Delisle, G., Merchel, S., and Ott, U. (2010). Glaciation history of Queen Maud Land (Antarctica) reconstructed from in-situ produced cosmogenic 10Be, 26Al and 21Ne. Polar Science 4, 42–61.
CrossRef |

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
| CAS |

Andrassy, I. (1998). Nematodes in the sixth continent. Journal of Nematode Systematics and Morphology 1, 107–108.

Ashworth, A. C. C., and Cantrill, D. (2004). Neogene vegetation of the Meyer Desert Formation (Sirius Group) Transantarctic Mountains, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 213, 65–82.

Ashworth, A. C. C., and Thompson, C. F. (2003). A fly in the biogeographic ointment. Nature 423, 135–136.
CrossRef | CAS |

Bentley, M. J. (2010). The Antarctic palaeo record and its role in improving predictions of future Antarctic Ice Sheet change. Journal of Quaternary Science 25, 5–18.
CrossRef |

Bentley, M. J., Hodgson, D. A., Smith, J. A., Cofaigh, C. Ó., Domack, E. W., Larter, R. D., Roberts, S. J., Brachfeld, S., Leventer, A., Hjort, C., Hillenbrand, C.-D., and Evans, J. (2009). Mechanisms of Holocene palaeoenvironmental change in the Antarctic Peninsula region. The Holocene 19, 51–69.
CrossRef |

Bertolani, R., Biserov, V., Rebecchi, L., and Cesari, M. (2011). Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology 8, 23–36.

Cesari, M., Bertolani, R., Rebecchi, L., and Guidetti, R. (2009). DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Molecular Ecology Resources 9, 699–706.
CrossRef | CAS |

Cesari, M., Giovannini, I., Bertolani, R., and Rebecchi, L. (2011). An example of problems associated with DNA barcoding in tardigrades: a novel method for obtaining voucher specimens. Zootaxa 3104, 42–51.

Chown, S. L., and Convey, P. (2007). Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 362, 2307–2331.
CrossRef |

Clarke, A., and Crame, J. A. (1989). The origin of the Southern Ocean marine fauna. Geological Society of London, Special Publications 47, 253–268.
CrossRef |

Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
CrossRef | CAS |

Convey, P., and McInnes, S. J. (2005). Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica. Ecology 86, 519–527.
CrossRef |

Convey, P., and Stevens, M. I. (2007). Antarctic biodiversity. Science 317, 1877–1878.
CrossRef | CAS |

Convey, P., Gibson, J. E., Hillenbrand, C. D., Hodgson, D. A., Pugh, P. J. A., Smellie, J. L., and Stevens, M. I. (2008). Antarctic terrestrial life – challenging the history of the frozen continent? Biological Reviews of the Cambridge Philosophical Society 83, 103–117.
CrossRef |

Convey, P., Stevens, M. I., Dominic, A. H., Smellie, J. L., Hillenbrand, C. D., Barnes, D. K. A., Clarke, A., Pugh, P. J. A., Linse, K., and Cary, S. C. (2009). Exploring biological constraints on the glacial history of Antarctica. Quaternary Science Reviews 28, 3035–3048.
CrossRef |

Cromer, L., Gibson, J. A. E., McInnes, S. J., and Agius, J. T. (2008). Tardigrade remains from lake sediments. Journal of Paleolimnology 39, 143–150.
CrossRef |

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics (Oxford, England) 27, 1164–1165.
CrossRef | CAS |

Davis, R. C. (1981). Structure and function of two Antarctic terrestrial moss communities. Ecological Monographs 51, 125–143.
CrossRef |

Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2012). Geneious v.5.6.4. Available from http://www.geneious.com.

Francis, J. E. (1986). Growth rings in Cretaceous and Tertiary wood from Antarctica and their palaeoclimatic implications. Palaeontology 29, 665–684.

Francis, J. E., and Poole, I. (2002). Cretaceous and early Tertiary climates of Antarctica: evidence from fossil wood. Palaeogeography, Palaeoclimatology, Palaeoecology 182, 47–64.
CrossRef |

Freckman, D. W., and Virginia, R. A. (1993). Extraction of nematodes from Dry Valley Antarctic soils. Polar Biology 13, 483–487.
CrossRef |

Garrick, R. C., Sands, J., Rowell, D. M., Hillis, D. M., and Sunnucks, P. (2007). Catchments catch all: long-term population history of a giant springtail from the southeast Australian highlands—a multigene approach. Molecular Ecology 16, 1865–1882.
| CAS |

Gibson, J. A. E., Cromer, L., Agius, J. T., McInnes, S. J., and Marley, N. J. (2007). Tardigrade eggs and exuviae in Antarctic lake sediments: insights into Holocene dynamics and origins of the fauna. Journal of Limnology 66, 65–71.
CrossRef |

Gu, X., Fu, Y. X., and Li, W. H. (1995). Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Molecular Biology and Evolution 12, 546–557.
| CAS |

Hart, M. W., and Sunday, J. (2007). Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3, 509–512.
CrossRef | CAS |

Hills, S. F., Stevens, M. I., and Gemmill, C. E. C. (2010). Molecular support for Pleistocene persistence of the continental Antarctic moss Bryum argenteum. Antarctic Science 22, 721–726.
CrossRef |

Huson, D. H., Richter, D. C., Rausch, C., Dezulian, T., Franz, M., and Rupp, R. (2007). Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460.
CrossRef |

Joly, S., Stevens, M. I., and Jansen van Vuuren, B. (2007). Haplotype networks can be misleading in the presence of missing data. Systematic Biology 56, 857–862.
CrossRef |

Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). A new approach to protein fold recognition. Nature 358, 86–89.
CrossRef | CAS |

Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286–298.
CrossRef | CAS |

Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
CrossRef | CAS |

Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.
CrossRef | CAS |

Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
CrossRef | CAS |

Lawver, L. A., and Gahagan, L. M. (2003). Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeography, Palaeoclimatology, Palaeoecology 198, 11–37.
CrossRef |

Livermore, R., Hillenbrand, C.-D., Meredith, M., and Eagles, G. (2007). Drake Passage and Cenozoic climate: an open and shut case? Geochemistry Geophysics Geosystems 8, Q01005.
CrossRef |

Magalhães, C., Stevens, M. I., Cary, S. C., Ball, B. A., Storey, B. C., Wall, D. H., Türk, R., and Ruprecht, U. (2012). At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in continental Antarctica. PLoS ONE 7, e44578.
CrossRef |

Marley, N. J., McInnes, S. J., and Sands, C. J. (2011). Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 64, 51–64.

McGaughran, A., Stevens, M. I., and Holland, B. R. (2010). Biogeography of circum-Antarctic springtails. Molecular Phylogenetics and Evolution 57, 48–58.
CrossRef |

McGaughran, A., Stevens, M. I., Hogg, I. D., and Carapelli, A. (2011). Extreme glacial legacies: a synthesis of the Antarctic springtail phylogeographic record. Insects 2, 62–82.
CrossRef |

McInnes, S. J. (1994). Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal of Natural History 28, 257–352.
CrossRef |

McInnes, S. J., and Pugh, P. J. A. (1998). Biogeography of limno-terrestrial Tardigrada, with particular reference to the Antarctic fauna. Journal of Biogeography 25, 31–36.
CrossRef |

McInnes, S. J., and Pugh, P. J. A. (2007). An attempt to revisit the global biogeography of limno-terrestrial Tardigrada. Journal of Limnology 66, 90–96.
CrossRef |

Mortimer, E., Jansen van Vuuren, B., Lee, J. E., Marshall, D. J., Convey, P., and Chown, S. L. (2011). Mite dispersal among the Southern Ocean islands and Antarctica before the last glacial maximum. Proceedings of The Royal Society of London, Biological sciences 278, 1247–1255.
| CAS |

Nelson, D. R. (2002). Current status of the Tardigrada: evolution and ecology. Integrative and Comparative Biology 42, 652–659.
CrossRef |

Niederhauser, C., Höfelein, C., Wegmüller, B., Lüthy, J., and Candrian, U. (1994). Reliability of PCR decontamination systems. PCR Methods and Applications 4, 117–123.
CrossRef | CAS |

Nkem, J. N., Wall, D. H., Virginia, R. A., Barrett, J. E., Broos, E. J., Porazinska, D. L., and Adams, B. J. (2006). Wind dispersal of soil invertebrates in the McMurdo Dry valleys, Antarctica. Polar Biology 29, 346–352.
CrossRef |

Ottesen, P. S., and Meier, T. (1990). Tardigrada from the Husvik area, South Georgia, sub-Antarctic. Polar Research 8, 291–294.
CrossRef |

Pfuhl, H., and McCave, I. (2005). Evidence for late Oligocene establishment of the Antarctic Circumpolar Current. Earth and Planetary Science Letters 235, 715–728.
CrossRef | CAS |

Pilato, G., and Binda, M. G. (2001). Biogeography and limno-terrestrial tardigrades: are they truly incompatible binomials? Zoologischer Anzeiger – A Journal of Comparative Zoology 240, 511–516.

Pilato, G., and Binda, M. G. (2010). Definition of families, subfamilies, genera and subgenera of the Eutardigrada, and keys to their identification. Zootaxa 2404, 1–54.

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
CrossRef | CAS |

Pugh, P. J. A. (1993). A synonymic catalogue of the Acari from Antarctica, the sub-Antarctic Islands and the Southern Ocean. Journal of Natural History 27, 323–421.
CrossRef |

Pugh, P. J. A., and McInnes, S. J. (1998). The origin of Arctic terrestrial and freshwater tardigrades. Polar Biology 19, 177–182.
CrossRef |

Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.
CrossRef | CAS |

Saiki, R., Gelfand, D., Stoffel, S., Scharf, S., Higuchi, R., Horn, G., Mullis, K., and Erlich, H. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487–491.
CrossRef | CAS |

Sands, C. J., McInnes, S. J., Marley, N. J., Goodall-Copestake, W. P., Convey, P., and Linse, K. (2008a). Phylum Tardigrada: an ‘individual’ approach. Cladistics 24, 861–871.
CrossRef |

Sands, C. J., Convey, P., Linse, K., and McInnes, S. J. (2008b). Assessing meiofaunal variation among individuals utilising morphological and molecular approaches: an example using the Tardigrada. BMC Ecology 8, 7.
CrossRef |

Scher, H. D., and Martin, E. E. (2006). Timing and climatic consequences of the opening of Drake Passage. Science 312, 428–430.
CrossRef | CAS |

Sohlenius, B., and Boström, S. (2005). The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28, 439–448.
CrossRef |

Sohlenius, B., and Boström, S. (2006). Patch-dynamics and population structure of nematodes and tardigrades on Antarctic nunataks. European Journal of Soil Biology 42, S321–S325.
CrossRef |

Sohlenius, B., Boström, S., and Hirschfelder, A. (1995). Nematodes, rotifers and tardigrades from nunataks in Dronning Maud Land, East Antarctica. Polar Biology 15, 51–56.
CrossRef |

Sohlenius, B., Boström, S., and Hirschfelder, A. (1996). Distribution patterns of microfauna (nematodes, rotifers and tardigrades) on nunataks in Dronning Maud Land, East Antarctica. Polar Biology 16, 191–200.
CrossRef |

Sohlenius, B., Boström, S., and Jönsson, K. I. (2004). Occurrence of nematodes, tardigrades and rotifers on ice-free areas in East Antarctica. Pedobiologia 48, 395–408.
CrossRef |

Sømme, L., and Meier, T. (1995). Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica. Polar Biology 15, 221–224.
CrossRef |

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688–2690.
CrossRef | CAS |

Stevens, M. I., and Hogg, I. D. (2002). Expanded distributional records of Collembola and Acari in southern Victoria Land, Antarctica. Pedobiologia 46, 485–495.
CrossRef |

Stevens, M. I., and Hogg, I. D. (2003). Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica. Molecular Ecology 12, 2357–2369.
CrossRef | CAS |

Stevens, M. I., and Hogg, I. D. (2006). Contrasting levels of mitochondrial DNA variability between mites (Penthalodidae) and springtails (Hypogastruridae) from the Trans-Antarctic Mountains suggest long-term effects of glaciation and life history on substitution rates, and speciation processes. Soil Biology & Biochemistry 38, 3171–3180.
CrossRef | CAS |

Stevens, M. I., Greenslade, P., Hogg, I. D., and Sunnucks, P. (2006). Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Molecular Biology and Evolution 23, 874–882.
CrossRef | CAS |

Stevens, M. I., Porco, D., D’Haese, C. A., and Deharveng, L. (2011). Comment on “Taxonomy and the DNA Barcoding Enterprise” by Ebach (2011). Zootaxa 2838, 85–88.

Storey, B. C., Fink, D., Hood, D., Joy, K., Shulmeister, J., Riger-Kusk, M., and Stevens, M. I. (2010). Cosmogenic nuclide exposure age constraints on the glacial history and implications on biogeography of the Lake Wellman area, Darwin Mountains, Antarctica. Antarctic Science 22, 603–618.
CrossRef |

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
CrossRef | CAS |

Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17, 57–86.

Whitehead, J. M. M., Quilty, P. G. G., Mckelvey, B. C. C., and O’Brien, P. E. (2006). A review of the cenozoic stratigraphy and glacial history of the Lambert Graben – Prydz Bay Region, East Antarctica. Antarctic Science 18, 83–99.
CrossRef |

Wright, J. C. (2001). Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zoologischer Anzeiger – A Journal of Comparative Zoology 240, 563–582.

Wright, J. C., Westh, P., and Ramløv, H. (1992). Cryptobiosis in Tardigrada. Biological Reviews of the Cambridge Philosophical Society 67, 1–29.
CrossRef |

Yang, Z. (1993). Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Molecular Biology and Evolution 10, 1396–1401.
| CAS |

Yang, Z. (1998). On the best evolutionary rate for phylogenetic analysis. Systematic Biology 47, 125–133.
CrossRef | CAS |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014