Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

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

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.
Diversity and distribution of Victoria Land biota.CrossRef | 1:CAS:528:DC%2BD28XpvFegurs%3D&md5=78db7679812f5471620bee0323aae30bCAS | open url image1

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.
The southernmost worm, Scottnema lindsayae (Nematoda): diversity, dispersal and ecological stability.CrossRef | open url image1

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.
Glaciation history of Queen Maud Land (Antarctica) reconstructed from in-situ produced cosmogenic 10Be, 26Al and 21Ne.CrossRef | open url image1

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.
| 1:CAS:528:DyaK3MXitVGmsA%3D%3D&md5=97d289603d93f29ea063daa461aa774dCAS | open url image1

Andrassy, I. (1998). Nematodes in the sixth continent. Journal of Nematode Systematics and Morphology 1, 107–108. open url image1

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. open url image1

Ashworth, A. C. C., and Thompson, C. F. (2003). A fly in the biogeographic ointment. Nature 423, 135–136.
A fly in the biogeographic ointment.CrossRef | 1:CAS:528:DC%2BD3sXjsVOrsbs%3D&md5=e7ce212e27817dd021762c2fca65937cCAS | open url image1

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.
The Antarctic palaeo record and its role in improving predictions of future Antarctic Ice Sheet change.CrossRef | open url image1

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.
Mechanisms of Holocene palaeoenvironmental change in the Antarctic Peninsula region.CrossRef | open url image1

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. open url image1

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.
DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae).CrossRef | 1:CAS:528:DC%2BD1MXls1Ggtb4%3D&md5=01c9a0eed7aa4945ef3b6d6707f2b08eCAS | open url image1

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. open url image1

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.
Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic.CrossRef | open url image1

Clarke, A., and Crame, J. A. (1989). The origin of the Southern Ocean marine fauna. Geological Society of London, Special Publications 47, 253–268.
The origin of the Southern Ocean marine fauna.CrossRef | open url image1

Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS: a computer program to estimate gene genealogies.CrossRef | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=212c00f91e7809668dc578c7ebdd4da2CAS | open url image1

Convey, P., and McInnes, S. J. (2005). Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica. Ecology 86, 519–527.
Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica.CrossRef | open url image1

Convey, P., and Stevens, M. I. (2007). Antarctic biodiversity. Science 317, 1877–1878.
Antarctic biodiversity.CrossRef | 1:CAS:528:DC%2BD2sXhtFamtLbN&md5=ccb3db0591791388e2f5e21ed6bee176CAS | open url image1

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.
Antarctic terrestrial life – challenging the history of the frozen continent?CrossRef | open url image1

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.
Exploring biological constraints on the glacial history of Antarctica.CrossRef | open url image1

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.
Tardigrade remains from lake sediments.CrossRef | open url image1

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.
ProtTest 3: fast selection of best-fit models of protein evolution.CrossRef | 1:CAS:528:DC%2BC3MXksFKltbs%3D&md5=468e857ba44ce72dfb9d01ce92d60093CAS | open url image1

Davis, R. C. (1981). Structure and function of two Antarctic terrestrial moss communities. Ecological Monographs 51, 125–143.
Structure and function of two Antarctic terrestrial moss communities.CrossRef | open url image1

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. open url image1

Francis, J. E., and Poole, I. (2002). Cretaceous and early Tertiary climates of Antarctica: evidence from fossil wood. Palaeogeography, Palaeoclimatology, Palaeoecology 182, 47–64.
Cretaceous and early Tertiary climates of Antarctica: evidence from fossil wood.CrossRef | open url image1

Freckman, D. W., and Virginia, R. A. (1993). Extraction of nematodes from Dry Valley Antarctic soils. Polar Biology 13, 483–487.
Extraction of nematodes from Dry Valley Antarctic soils.CrossRef | open url image1

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.
| 1:STN:280:DC%2BD2s3js1Gjug%3D%3D&md5=14ecebdae177f1073e7c63f52556f452CAS | open url image1

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.
Tardigrade eggs and exuviae in Antarctic lake sediments: insights into Holocene dynamics and origins of the fauna.CrossRef | open url image1

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.
| 1:CAS:528:DyaK2MXmsVOqsrc%3D&md5=5eb5561c977351878f20a8b6844c7e9dCAS | open url image1

Hart, M. W., and Sunday, J. (2007). Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3, 509–512.
Things fall apart: biological species form unconnected parsimony networks.CrossRef | 1:CAS:528:DC%2BD2sXhtF2hs77K&md5=64d60f42d41cafaa960a38222a34c383CAS | open url image1

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.
Molecular support for Pleistocene persistence of the continental Antarctic moss Bryum argenteum.CrossRef | open url image1

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.
Dendroscope: an interactive viewer for large phylogenetic trees.CrossRef | open url image1

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.
Haplotype networks can be misleading in the presence of missing data.CrossRef | open url image1

Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). A new approach to protein fold recognition. Nature 358, 86–89.
A new approach to protein fold recognition.CrossRef | 1:CAS:528:DyaK38Xks1Kjsbc%3D&md5=7a6b522ac627edd670156be65dbbd285CAS | open url image1

Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286–298.
Recent developments in the MAFFT multiple sequence alignment program.CrossRef | 1:CAS:528:DC%2BD1cXpt1artrs%3D&md5=ca087e9f390fcf4f6dde79794bbf9259CAS | open url image1

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.
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.CrossRef | 1:CAS:528:DC%2BD38XlslOqu7s%3D&md5=9ce820f79aaf32554a07c7b60b3f4d5bCAS | open url image1

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.
MAFFT version 5: improvement in accuracy of multiple sequence alignment.CrossRef | 1:CAS:528:DC%2BD2MXhtV2qsbc%3D&md5=ac9f0a07531f49f2daa716d9416d5216CAS | open url image1

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.
A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences.CrossRef | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=78555c3dc7e755aed13a5a2a8c5b8747CAS | open url image1

Lawver, L. A., and Gahagan, L. M. (2003). Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeography, Palaeoclimatology, Palaeoecology 198, 11–37.
Evolution of Cenozoic seaways in the circum-Antarctic region.CrossRef | open url image1

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.
Drake Passage and Cenozoic climate: an open and shut case?CrossRef | open url image1

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.
At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in continental Antarctica.CrossRef | open url image1

Marley, N. J., McInnes, S. J., and Sands, C. J. (2011). Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 64, 51–64. open url image1

McGaughran, A., Stevens, M. I., and Holland, B. R. (2010). Biogeography of circum-Antarctic springtails. Molecular Phylogenetics and Evolution 57, 48–58.
Biogeography of circum-Antarctic springtails.CrossRef | open url image1

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.
Extreme glacial legacies: a synthesis of the Antarctic springtail phylogeographic record.CrossRef | open url image1

McInnes, S. J. (1994). Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal of Natural History 28, 257–352.
Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature.CrossRef | open url image1

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.
Biogeography of limno-terrestrial Tardigrada, with particular reference to the Antarctic fauna.CrossRef | open url image1

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.
An attempt to revisit the global biogeography of limno-terrestrial Tardigrada.CrossRef | open url image1

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.
| 1:STN:280:DC%2BC3M3lvFelsQ%3D%3D&md5=73d2895d521c3c2f557b9dad46750c20CAS | open url image1

Nelson, D. R. (2002). Current status of the Tardigrada: evolution and ecology. Integrative and Comparative Biology 42, 652–659.
Current status of the Tardigrada: evolution and ecology.CrossRef | open url image1

Niederhauser, C., Höfelein, C., Wegmüller, B., Lüthy, J., and Candrian, U. (1994). Reliability of PCR decontamination systems. PCR Methods and Applications 4, 117–123.
Reliability of PCR decontamination systems.CrossRef | 1:CAS:528:DyaK2MXhslGkt7w%3D&md5=76444d7f554a8f62b3fadb1811dba056CAS | open url image1

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.
Wind dispersal of soil invertebrates in the McMurdo Dry valleys, Antarctica.CrossRef | open url image1

Ottesen, P. S., and Meier, T. (1990). Tardigrada from the Husvik area, South Georgia, sub-Antarctic. Polar Research 8, 291–294.
Tardigrada from the Husvik area, South Georgia, sub-Antarctic.CrossRef | open url image1

Pfuhl, H., and McCave, I. (2005). Evidence for late Oligocene establishment of the Antarctic Circumpolar Current. Earth and Planetary Science Letters 235, 715–728.
Evidence for late Oligocene establishment of the Antarctic Circumpolar Current.CrossRef | 1:CAS:528:DC%2BD2MXlvVCrt7o%3D&md5=0a25c3e9a8b7504c1180a5a726f22b6eCAS | open url image1

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. open url image1

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. open url image1

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.CrossRef | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=8a1f07129ca906c4b292e237699ed9deCAS | open url image1

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.
A synonymic catalogue of the Acari from Antarctica, the sub-Antarctic Islands and the Southern Ocean.CrossRef | open url image1

Pugh, P. J. A., and McInnes, S. J. (1998). The origin of Arctic terrestrial and freshwater tardigrades. Polar Biology 19, 177–182.
The origin of Arctic terrestrial and freshwater tardigrades.CrossRef | open url image1

Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.
MRBAYES 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=9c53a6e1009ac0a4829f70ecd07199e1CAS | open url image1

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.
Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.CrossRef | 1:CAS:528:DyaL1cXht1Ogt7k%3D&md5=f50f91c42d0a59487e1936b3daa596a7CAS | open url image1

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.
Phylum Tardigrada: an ‘individual’ approach.CrossRef | open url image1

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.
Assessing meiofaunal variation among individuals utilising morphological and molecular approaches: an example using the Tardigrada.CrossRef | open url image1

Scher, H. D., and Martin, E. E. (2006). Timing and climatic consequences of the opening of Drake Passage. Science 312, 428–430.
Timing and climatic consequences of the opening of Drake Passage.CrossRef | 1:CAS:528:DC%2BD28XjslSktLc%3D&md5=ed50528384633b76fc3c21b22ee72b1fCAS | open url image1

Sohlenius, B., and Boström, S. (2005). The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28, 439–448.
The geographic distribution of metazoan microfauna on East Antarctic nunataks.CrossRef | open url image1

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.
Patch-dynamics and population structure of nematodes and tardigrades on Antarctic nunataks.CrossRef | open url image1

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.
Nematodes, rotifers and tardigrades from nunataks in Dronning Maud Land, East Antarctica.CrossRef | open url image1

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.
Distribution patterns of microfauna (nematodes, rotifers and tardigrades) on nunataks in Dronning Maud Land, East Antarctica.CrossRef | open url image1

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.
Occurrence of nematodes, tardigrades and rotifers on ice-free areas in East Antarctica.CrossRef | open url image1

Sømme, L., and Meier, T. (1995). Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica. Polar Biology 15, 221–224.
Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica.CrossRef | open url image1

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models.CrossRef | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=b87f90ecd58defc1de3c5b475255c579CAS | open url image1

Stevens, M. I., and Hogg, I. D. (2002). Expanded distributional records of Collembola and Acari in southern Victoria Land, Antarctica. Pedobiologia 46, 485–495.
Expanded distributional records of Collembola and Acari in southern Victoria Land, Antarctica.CrossRef | open url image1

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.
Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica.CrossRef | 1:CAS:528:DC%2BD3sXnvVSgt70%3D&md5=9bcf34642a5d40370879ef5c9ba1adbfCAS | open url image1

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.
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.CrossRef | 1:CAS:528:DC%2BD28XpvFens7s%3D&md5=d67678824613ee96eec1295dc239a198CAS | open url image1

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.
Southern Hemisphere springtails: could any have survived glaciation of Antarctica?CrossRef | 1:CAS:528:DC%2BD28XkvVeqtLg%3D&md5=e8d7cae2d8f2032d6b654c6f12c88ee5CAS | open url image1

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. open url image1

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.
Cosmogenic nuclide exposure age constraints on the glacial history and implications on biogeography of the Lake Wellman area, Darwin Mountains, Antarctica.CrossRef | open url image1

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.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=ff48f25899fc988f16ef1534cf14445fCAS | open url image1

Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17, 57–86. open url image1

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.
A review of the cenozoic stratigraphy and glacial history of the Lambert Graben – Prydz Bay Region, East Antarctica.CrossRef | open url image1

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. open url image1

Wright, J. C., Westh, P., and Ramløv, H. (1992). Cryptobiosis in Tardigrada. Biological Reviews of the Cambridge Philosophical Society 67, 1–29.
Cryptobiosis in Tardigrada.CrossRef | open url image1

Yang, Z. (1993). Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Molecular Biology and Evolution 10, 1396–1401.
| 1:CAS:528:DyaK2cXisF2gsA%3D%3D&md5=ea1a0c49660c81fed801e92714e731cfCAS | open url image1

Yang, Z. (1998). On the best evolutionary rate for phylogenetic analysis. Systematic Biology 47, 125–133.
On the best evolutionary rate for phylogenetic analysis.CrossRef | 1:STN:280:DC%2BD38zitVKktw%3D%3D&md5=7137a3d73ae03ec50b74938651936679CAS | open url image1



Supplementary MaterialSupplementary Material 11.57 MB Export Citation