Genetic diversity and biogeography of the south polar water bear Acutuncus antarcticus (Eutardigrada : Hypsibiidae) – evidence that it is a truly pan-Antarctic species
Michele Cesari A , Sandra J. McInnes B , Roberto Bertolani A , Lorena Rebecchi A C and Roberto Guidetti A
+ Author Affiliations
- Author Affiliations
A Department of Life Sciences, University of Modena and Reggio Emilia, via G. Campi 213/d, 41125, Modena, Italy.
B British Antarctic Survey, Natural Environment Research Council, Madingley Road, Cambridge, CB3 0ET, UK.
C Corresponding author. Email: lorena.rebecchi@unimore.it
Invertebrate Systematics 30(6) 635-649 https://doi.org/10.1071/IS15045
Submitted: 15 October 2015 Accepted: 30 May 2016 Published: 13 December 2016
Abstract
Antarctica is an ice-dominated continent and all its terrestrial and freshwater habitats are fragmented, which leads to genetic divergence and, eventually, speciation. Acutuncus antarcticus is the most common Antarctic tardigrade and its cryptobiotic capabilities, small size and parthenogenetic reproduction present a high potential for dispersal and colonisation. Morphological (light and electron microscopy, karyology) and molecular (18S rRNA and cytochrome c oxidase subunit I (COI) genes) analyses on seven populations of A. antarcticus elucidated the genetic diversity and distribution of this species. All analysed populations were morphologically indistinguishable and made up of diploid females. All specimens presented the same 18S rRNA sequence. In contrast, COI analysis showed higher variability, with most Victoria Land populations presenting up to five different haplotypes. Genetic distances between Victoria Land specimens and those found elsewhere in Antarctica were low, while distances between Dronning Maud Land and specimens from elsewhere were high. Our analyses show that A. antarcticus can still be considered a pan-Antarctic species, although the moderately high genetic diversity within Victoria Land indicates the potential for speciation events. Regions of Victoria Land are considered to have been possible refugia during the last glacial maximum and a current biodiversity hotspot, which the populations of A. antarcticus mirror with a higher diversity than in other regions of Antarctica.
References
Allegrucci, G., Carchini, G., Convey, P., and Sbordoni, V. (2012). Evolutionary geographic relationships among orthocladine chironomid midges from maritime Antarctic and sub-Antarctic islands. Biological Journal of the Linnean Society. Linnean Society of London 106, 258–274.| Evolutionary geographic relationships among orthocladine chironomid midges from maritime Antarctic and sub-Antarctic islands.Crossref | GoogleScholarGoogle Scholar |
Altiero, T., Giovannini, I., Guidetti, R., and Rebecchi, L. (2015). Life history traits and reproductive mode of the tardigrade Acutuncus antarcticus under laboratory conditions: strategies to colonize the Antarctic environment. Hydrobiologia 761, 277–291.
| Life history traits and reproductive mode of the tardigrade Acutuncus antarcticus under laboratory conditions: strategies to colonize the Antarctic environment.Crossref | GoogleScholarGoogle Scholar |
Barnes, D. K. A., Hodgson, D. A., Convey, P., Allen, C. S., and Clarke, A. (2006). Incursion and excursion of Antarctic biota: past, present and future. Global Ecology and Biogeography 15, 121–142.
| Incursion and excursion of Antarctic biota: past, present and future.Crossref | GoogleScholarGoogle Scholar |
Bergstrom, D. M., and Chown, S. L. (1999). Life at the front: history, ecology and change on Southern Ocean islands. Trends in Ecology & Evolution 14, 472–477.
| Life at the front: history, ecology and change on Southern Ocean islands.Crossref | GoogleScholarGoogle Scholar |
Bertolani, R. (2001). Evolution of the reproductive mechanisms in Tardigrades – a review. Zoologischer Anzeiger 240, 247–252.
| Evolution of the reproductive mechanisms in Tardigrades – a review.Crossref | GoogleScholarGoogle Scholar |
Bertolani, R., Rebecchi, L., Giovannini, I., and Cesari, M. (2011a). DNA barcoding and integrative taxonomy of Macrobiotus hufelandi C.A.S. Schultze 1834, the first tardigrade species to be described, and some related species. Zootaxa 2997, 19–36.
Bertolani, R., Biserov, V. I., Rebecchi, L., and Cesari, M. (2011b). Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology 8, 23–36.
Bertolani, R., Guidetti, R., Marchioro, T., Altiero, T., Rebecchi, L., and Cesari, M. (2014). Phylogeny of Eutardigrada: new molecular data and their morphological support lead to the identification of new evolutionary lineages. Molecular Phylogenetics and Evolution 76, 110–126.
| Phylogeny of Eutardigrada: new molecular data and their morphological support lead to the identification of new evolutionary lineages.Crossref | GoogleScholarGoogle Scholar |
Block, W. (1984). Terrestrial microbiology, invertebrates and ecosystems. In ‘Antarctic Ecology’. (Ed. R. M. Laws.) Volume 1, pp. 163–236. (Academic Press: London, UK.)
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=7270e7b94b46ec4a30ad5328609b8552CAS |
Cesari, M., Luchetti, A., Scanabissi, F., and Mantovani, B. (2007). Genetic variability in European Leptestheria dahalacensis (Rüppel, 1837) (Crustacea, Branchiopoda, Spinicaudata). Hydrobiologia 586, 249–260.
| Genetic variability in European Leptestheria dahalacensis (Rüppel, 1837) (Crustacea, Branchiopoda, Spinicaudata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltl2hsbc%3D&md5=bbdf824e333e8291934ec633789165a8CAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1Ggtb4%3D&md5=a13fa489f4adc9f0ac85156471992d4fCAS |
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.
Cesari, M., Guidetti, R., Rebecchi, L., Giovannini, I., and Bertolani, R. (2013). A DNA barcoding approach in the study of tardigrades. Journal of Limnology 72, 182–198.
| A DNA barcoding approach in the study of tardigrades.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=e49e12cd98564c97d93802097f5a4308CAS |
Convey, P. (2001). Antarctic ecosystems. In ‘Encyclopaedia of Biodiversity’. (Ed. A. Levion.) pp. 171–184. (Academic Press: San Diego, CA.)
Convey, P. (2010). Terrestrial biodiversity in Antarctica – recent advances and future challenges. Polar Science 4, 135–147.
| Terrestrial biodiversity in Antarctica – recent advances and future challenges.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Convey, P., and Stevens, M. I. (2007). Antarctic biodiversity. Science 317, 1877–1878.
| Antarctic biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFamtLbN&md5=145a8a4a9680f5a4ec79ddd5d38e01c0CAS |
Convey, P., Gibson, J. A. E., Hillenbrand, C. D., Hodgson, D. A., Pugh, P. J. A., Smellie, J. L., and Stevens, M. (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 | GoogleScholarGoogle Scholar |
Convey, P., Stevens, M. I., Hodgson, D. A., 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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Czechowski, P., Sands, C. J., Adams, B. J., D’Haese, C. A., Gibson, J. A. E., McInnes, S. J., and Stevens, M. I. (2012). Antarctic Tardigrada: a first step in understanding molecular operational taxonomic units (MOTUs) and biogeography of cryptic meiofauna. Invertebrate Systematics 26, 526–538.
| Antarctic Tardigrada: a first step in understanding molecular operational taxonomic units (MOTUs) and biogeography of cryptic meiofauna.Crossref | GoogleScholarGoogle Scholar |
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=b326576d8549dc5561e70b14d1339c77CAS |
Dastych, H. (1991). Redescription of Hypsibius antarcticus (Richters, 1904), with some notes on Hypsibius arcticus (Murray, 1907) (Tardigrada). Mitteilungen aus den Hamburgischen Zoologischen Museum und Institut 88, 141–159.
Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |
Faurby, S., Jönsson, K. I., Rebecchi, L., and Funch, P. (2008). Variation in anhydrobiotic survival of two eutardigrade morphospecies: a story of cryptic species and their dispersal. Journal of Zoology 275, 139–145.
| Variation in anhydrobiotic survival of two eutardigrade morphospecies: a story of cryptic species and their dispersal.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=3ed3b40952948838a8ebb6c4cd36ee0cCAS |
Fraser, C. I., Nikula, R., Ruzzante, D. E., and Waters, J. M. (2012). Poleward bound: biological impacts of southern hemisphere glaciations. Trends in Ecology & Evolution 27, 462–471.
| Poleward bound: biological impacts of southern hemisphere glaciations.Crossref | GoogleScholarGoogle Scholar |
Frisch, D., Green, A. J., and Figuerola, J. (2007). High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquatic Sciences 69, 568–574.
| High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds.Crossref | GoogleScholarGoogle Scholar |
Fu, Y. X. (1994). A phylogenetic estimator of effective population size or mutation rate. Genetics 136, 685–692.
| 1:STN:280:DyaK2c3gtVKjtA%3D%3D&md5=48085be605280810de5630d1c15311f3CAS |
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 | GoogleScholarGoogle Scholar |
Guidetti, R., Schill, R. O., Bertolani, R., Dandekar, T., and Wolf, M. (2009). New molecular data for tardigrade phylogeny, with the erection of Paramacrobiotus gen. nov. Journal of Zoological Systematics and Evolutionary Research 47, 315–321.
| New molecular data for tardigrade phylogeny, with the erection of Paramacrobiotus gen. nov.Crossref | GoogleScholarGoogle Scholar |
Guidetti, R., Altiero, T., and Rebecchi, L. (2011). On dormancy strategies in tardigrades. Journal of Insect Physiology 57, 567–576.
| On dormancy strategies in tardigrades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmslOqsro%3D&md5=5a2b981ea1d0b4dfa465b4858f568ffbCAS |
Guidetti, R., Peluffo, J. R., Rocha, A. M., Cesari, M., and Moly de Peluffo, M. C. (2013). The morphological and molecular analyses of a new South American urban tardigrade offer new insights on the biological meaning of the Macrobiotus hufelandi group of species (Tardigrada: Macrobiotidae). Journal of Natural History 47, 2409–2426.
| The morphological and molecular analyses of a new South American urban tardigrade offer new insights on the biological meaning of the Macrobiotus hufelandi group of species (Tardigrada: Macrobiotidae).Crossref | GoogleScholarGoogle Scholar |
Guidetti, R., Bonifacio, A., Altiero, T., Bertolani, R., and Rebecchi, L. (2015). Distribution of calcium and chitin in the tardigrade feeding apparatus in relation to its function and morphology. Integrative and Comparative Biology 55, 241–252.
| Distribution of calcium and chitin in the tardigrade feeding apparatus in relation to its function and morphology.Crossref | GoogleScholarGoogle Scholar |
Guil, N., and Giribet, G. (2009). Fine scale population structure in the Echiniscus blumi-canadensis series (Heterotardigrada, Tardigrada) in an Iberian mountain range – when morphology fails to explain genetic structure. Molecular Phylogenetics and Evolution 51, 606–613.
| Fine scale population structure in the Echiniscus blumi-canadensis series (Heterotardigrada, Tardigrada) in an Iberian mountain range – when morphology fails to explain genetic structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlslajsL0%3D&md5=f3bf0feee846490697aa9158e853247eCAS |
Guil, N., and Giribet, G. (2012). A comprehensive molecular phylogeny of tardigrades – adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28, 21–49.
| A comprehensive molecular phylogeny of tardigrades – adding genes and taxa to a poorly resolved phylum-level phylogeny.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2hs77K&md5=1eac0876a37e5c22f5e1e4994bc62c20CAS |
Huiskes, A. H. L., Convey, P., and Bergstrom, D. (2006). Trends in Antarctic terrestrial and limnetic ecosystems: Antarctica as a global indicator. In ‘Trends in Antarctic Terrestrial and Limnetic Ecosystems: Antarctica as a Global Indicator’. (Eds A. H. L. Huiskes, P. Convey and D. Bergstrom.) pp. 1–13. (Springer-Verlag: Heidelberg, Germany.)
Jørgensen, A., Møbjerg, N., and Kristensen, R. M. (2007). A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. Journal of Limnology 66, 77–83.
| A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area.Crossref | GoogleScholarGoogle Scholar |
Jørgensen, A., Faurby, S., Hansen, J. G., Møbjerg, N., and Kristensen, R. M. (2010). Molecular phylogeny of Arthrotardigrada (Tardigrada). Molecular Phylogenetics and Evolution 54, 1006–1015.
| Molecular phylogeny of Arthrotardigrada (Tardigrada).Crossref | GoogleScholarGoogle Scholar |
Jørgensen, A., Faurby, S., Persson, D. K., Halberg, K. A., Kristensen, R. M., and Møbjerg, N. (2013). Genetic diversity in the parthenogenetic reproducing tardigrade Echiniscus testudo (Heterotardigrada: Echiniscoidea). Journal of Limnology 72, 136–143.
| Genetic diversity in the parthenogenetic reproducing tardigrade Echiniscus testudo (Heterotardigrada: Echiniscoidea).Crossref | GoogleScholarGoogle Scholar |
Kagoshima, H., Imura, S., and Suzuki, A. C. (2013). Molecular and morphological analysis of an Antarctic tardigrade, Acutuncus antarcticus. Journal of Limnology 72, 15–23.
| Molecular and morphological analysis of an Antarctic tardigrade, Acutuncus antarcticus.Crossref | GoogleScholarGoogle Scholar |
Kiehl, E. T., Dastych, H., D’Haese, J., and Greven, H. (2007). The 18S rRNA sequences support polyphyly of the Hypsibiidae (Eutardigrada). Journal of Limnology 66, 21–25.
| The 18S rRNA sequences support polyphyly of the Hypsibiidae (Eutardigrada).Crossref | GoogleScholarGoogle Scholar |
Lewis, A. R., Marchant, D. R., Ashworth, A. C., Hedenäs, L., Hemming, S. R., Johnson, J. V., Leng, M. J., Machlus, M. L., Newton, A. E., Raine, J. E., Willenbring, J. K., Williams, M., and Wolfe, A. P. (2008). Mid-Miocene cooling and the extinction of tundra in continental Antarctica. Proceedings of the National Academy of Sciences of the United States of America 105, 10676–10680.
| Mid-Miocene cooling and the extinction of tundra in continental Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvFSntLg%3D&md5=654fe4e37a0d5fd177bacfd34979e21fCAS |
Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=106edebfeb16e2122e13f701b6a1fea0CAS |
Marcus, E. (1928). Bärtierchen (Tardigrada). In ‘Die Tierwelt Deutschlands’. (Ed. F. Dahl.) Volume 12, 1–230. (Fischer: Jena, Germany)
Marley, N. J., McInnes, S. J., and Sands, C. J. (2011). Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 2819, 51–64.
McGaughran, A., Torricelli, G., Carapelli, A., Frati, F., Stevens, M. I., Convey, P., and Hogg, I. D. (2010). Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica. Journal of Biogeography 37, 103–119.
| Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica.Crossref | GoogleScholarGoogle Scholar |
McInnes, S. J. (1995). Tardigrades from Signy Island, South Orkney Islands, with particular reference to freshwater species. Journal of Natural History 29, 1419–1445.
| Tardigrades from Signy Island, South Orkney Islands, with particular reference to freshwater species.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Møbjerg, N., Halberg, K. A., Jorgensen, A., Persson, D., Bjorn, M., Ramlov, H., and Kristensen, R. M. (2011). Survival in extreme environments – on the current knowledge of adaptations in tardigrades. Acta Physiologica (Oxford, England) 202, 409–420.
| Survival in extreme environments – on the current knowledge of adaptations in tardigrades.Crossref | GoogleScholarGoogle Scholar |
Mortimer, E., Van Vuuren, B. J., 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. Biological Sciences 278, 1247–1255.
| Mite dispersal among the Southern Ocean Islands and Antarctica before the last glacial maximum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3lvFelsQ%3D%3D&md5=8d717c850dd2afe7a54841ec05c6d557CAS |
Murray, J. (1910). Tardigrada. Report of Scientific investigation of the British Antarctic Expedition, 1907–1909 (E.H. Shackleton) 1, 81–185. London.
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 | GoogleScholarGoogle Scholar |
Pilato, G., and Binda, M. G. (1997). Acutuncus, a new genus of Hypsibiidae (Eutardigrada). Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 12, 159–162.
Pilato, G., and Binda, M. G. (2001). Biogeography and limno-terrestrial tardigrades: are they truly incompatible binomials? Zoologischer Anzeiger 240, 511–516.
| Biogeography and limno-terrestrial tardigrades: are they truly incompatible binomials?Crossref | GoogleScholarGoogle Scholar |
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.
Pugh, P. J. A. (2004). Biogeography of spiders (Araneae: Arachnida) on the islands of the Southern Ocean. Journal of Natural History 38, 1461–1487.
| Biogeography of spiders (Araneae: Arachnida) on the islands of the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Pugh, P. J. A., and Convey, P. (2008). Surviving out in the cold: Antarctic endemic invertebrates and their refugia. Journal of Biogeography 35, 2176–2186.
| Surviving out in the cold: Antarctic endemic invertebrates and their refugia.Crossref | GoogleScholarGoogle Scholar |
Pugh, P. J. A., and Scott, B. (2002). Biodiversity and biogeography of non-marine Mollusca on the islands of the Southern Ocean. Journal of Natural History 36, 927–952.
| Biodiversity and biogeography of non-marine Mollusca on the islands of the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. J. (2007). Tracer v1.5. Available at: http://beast.bio.ed.ac.uk [Accessed on 2 November 2016]
Rebecchi, L., Altiero, T., and Bertolani, R. (2002). Banding techniques on tardigrade chromosomes: the karyotype of Macrobiotus richtersi (Eutardigrada, Macrobiotidae). Chromosome Research 10, 437–443.
| Banding techniques on tardigrade chromosomes: the karyotype of Macrobiotus richtersi (Eutardigrada, Macrobiotidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xotlektbk%3D&md5=3191d0801c76bcceab3e7b9384a6ade1CAS |
Richters, F. (1904). Vorläufiger Bericht über die anktartische Moosfauna. Verhandlungen der Deutschen Zoologischen Gesellschaft 14, 236–239.
Richters, F. (1908). Die fauna der moosrasen des Gaussbergs und einiger südlicher inseln. Deutsche Südpolar-Expedition 9, 259–302.
Richters, F. (1926). Tardigrada. In ‘Handbuch Zoologie. Volume 3’. (Eds W. Kükenthal and T. Krumbach.) pp. 1–68. (Walter de Gruyter & Co.: Berlin & Leipzig, Germany.)
Ritz, M. S., Millar, C., Miller, G. D., Phillips, R. A., Ryan, P., Sternkopf, V., Liebers-Helbig, D., and Peter, H. U. (2008). Phylogeography of the southern skua complex – rapid colonization of the southern hemisphere during a glacial period and reticulate evolution. Molecular Phylogenetics and Evolution 49, 292–303.
| Phylogeography of the southern skua complex – rapid colonization of the southern hemisphere during a glacial period and reticulate evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltr3J&md5=18e6d171af7fbb4b46ad18514202ed18CAS |
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Rossi, G., Claps, M., and Ardohain, D. (2009). Tardigrades from northwestern Patagonia (Neuquén Province, Argentina) with the description of three new species. Zootaxa 2095, 21–36.
Sands, C. J., McInnes, S. J., Marley, N. J., Goodall-Copestake, W. P., Convey, P., and Lindse, K. (2008). Phylum Tardigrada: an “individual” approach. Cladistics 24, 861–871.
| Phylum Tardigrada: an “individual” approach.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=75f7f4dcbee031d89a4fac72e69aca2fCAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvVeqtLg%3D&md5=719e133df031fb373def0c5aaeee66d6CAS |
Stevens, M. I., Frati, F., McGaughran, A., Spinsanti, G., and Hogg, I. D. (2007). Phylogeographic structure suggests multiple glacial refugia in northern Victoria Land for the endemic Antarctic springtail Desoria klovstadi (Collembola, Isotomidae). Zoologica Scripta 36, 201–212.
| Phylogeographic structure suggests multiple glacial refugia in northern Victoria Land for the endemic Antarctic springtail Desoria klovstadi (Collembola, Isotomidae).Crossref | GoogleScholarGoogle Scholar |
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 1:CAS:528:DyaK3cXhslentA%3D%3D&md5=598faf032e855ec8e49f142308ecb989CAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=00800be2ffa36aa51eab374da9e74db5CAS |
Tang, C. Q., Humphreys, A. M., Fontaneto, D., and Barraclough, T. G. (2014). Effects of phylogenetic reconstruction method of the robustness of species delimitation using single-locus data. Methods in Ecology and Evolution 5, 1086–1094.
| Effects of phylogenetic reconstruction method of the robustness of species delimitation using single-locus data.Crossref | GoogleScholarGoogle Scholar |
Templeton, A. R., Crandall, K. A., and Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
| 1:CAS:528:DyaK3sXhslSrsQ%3D%3D&md5=9bce65f69541e08d13d2814012941501CAS |
Torricelli, G., Carapelli, A., Convey, P., Nardi, F., Boore, J. L., and Frati, F. (2010). High divergence across the whole mitochondrial genome in the “pan-Antarctic” springtail Friesea grisea: evidence for cryptic species? Gene 449, 30–40.
| High divergence across the whole mitochondrial genome in the “pan-Antarctic” springtail Friesea grisea: evidence for cryptic species?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtleku7jK&md5=b8d0d4d39a9d7dcd5ed68d077f716ce8CAS |
Vyverman, W., Verleyen, E., Wilmotte, A., Hodgson, D. A., Willems, A., Peeters, K., Van de Vijver, B., De Wever, A., Leliaert, F., and Sabbe, K. (2010). Evidence for widespread endemism among Antarctic micro-organisms. Polar Science 4, 103–113.
| Evidence for widespread endemism among Antarctic micro-organisms.Crossref | GoogleScholarGoogle Scholar |
Wełnicz, W., Grohne, M. A., Kaczmarek, Ł., Schill, R. O., and Frohme, M. (2011). Anhydrobiosis in tardigrades – the last decade. Journal of Insect Physiology 57, 577–583.
| Anhydrobiosis in tardigrades – the last decade.Crossref | GoogleScholarGoogle Scholar |
Wright, S. (1969). ‘Evolution and the Genetics of Populations. Vol. 2: The Theory of Gene Frequencies.’ (University of Chicago Press: Chicago, IL.)
Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.
| A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWnsbzL&md5=35c688f3bd0ce12dfe0afb5164a00acdCAS |
