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Antarctic bdelloid rotifers: diversity, endemism and evolution

Abstract

Antarctica is an isolated continent whose conditions challenge the survival of living organisms. High levels of endemism are now known in many Antarctic organisms, including algae, tardigrades, nematodes and microarthropods. Bdelloid rotifers are a key, widespread and abundant group of Antarctic microscopic invertebrates. However, their diversity, regional distribution and endemism have received little attention until recently. We provide the first authoritative review on Antarctic Bdelloidea, based on published data and new collections. Our analysis reveals the extreme levels of bdelloid endemism in Antarctica. Sixty-six bdelloid morphospecies are now confirmed from the continent, and 83–91 putative species are identified using molecular approaches (depending on the delimitation method used). Twelve previously unknown species are described based on both morphology and molecular analyses. Molecular analyses indicate that only two putative species found in Antarctica proved to be truly cosmopolitan. The level of endemism based on the available data set (95%) is higher than that in any other continent, with many bdelloid species occurring only in maritime or continental Antarctica. These findings are consistent with the long-term presence of Bdelloidea in Antarctica, with their considerable isolation facilitating intraregional radiation, providing further evidence that does not support the microbial global ubiquity hypothesis that “everything is everywhere.”

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References

  • Adams, B. J., R. D. Bardgett, C. Ayres, D. H. Wall, J. Aislabie, S. Bamforth, R. Bargagli & S. C. Cary, 2006. Diversity and distribution of Victoria Land biota. Soil Biology and Biochemistry 38: 3003–3018.

    CAS  Article  Google Scholar 

  • Allegrucci, G., G. Carchini, P. Convey & V. Sbordoni, 2012. Evolutionary geographic relationships among chironomid midges from maritime Antarctic and sub-Antarctic islands. Biological Journal of the Linnean Society 106: 258–274.

    Article  Google Scholar 

  • Andrássy, I., 1998. Nematodes in the sixth continent. Journal of Nematode Systematics and Morphology 1: 107–186.

    Google Scholar 

  • Barraclough, T. G., D. Fontaneto, C. Ricci & E. A. Herniou, 2007. Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers. Molecular Biology and Evolution 24: 1952–1962.

    CAS  PubMed  Article  Google Scholar 

  • Bērziņš, B., 1987. Rotifer occurence in relation to pH. Hydrobiologia 147: 107–116.

    Article  Google Scholar 

  • Birky, C. W. & T. G. Barraclough, 2009. Asexual speciation. In Shön, I., K. Martens & P. Van Dijk (eds), Lost Sex: The evolutionary biology of parthenogenesis. Springer, Dordrecht: 201–216.

    Chapter  Google Scholar 

  • Birky, C. W., C. Wolf, H. Maughan, L. Herbertson & E. Henry, 2005. Speciation and selection without sex. Hydrobiologia 181: 29–45.

    Article  Google Scholar 

  • Birky, C. W., C. Ricci, G. Melone & D. Fontaneto, 2011. Integrating DNA and morphological taxonomy to describe diversity in poorly studied microscopic animals: new species of the genus Abrochtha Bryce, 1910 (Rotifera: Bdelloidea: Philodinavidae). Zoological Journal of the Linnean Society 161: 723–734.

    Article  Google Scholar 

  • Block, W., R. I. Lewis Smith & A. D. Kennedy, 2009. Strategies of survival and resource exploitation in the Antarctic fellfield ecosystem. Biological Reviews 84: 449–484.

    CAS  PubMed  Article  Google Scholar 

  • Bryce, D., 1894. Further notes on Macrotrachellous Callidinae. Journal of the Quekett Microscopical Club 5: 436–455.

    Article  Google Scholar 

  • Cathey, D. D., B. C. Parker, G. M. Simmons, W. H. Vongue & M. R. Van Brunt, 1981. The microfauna of algal mats and artificial substrates in Southern Victoria Land lakes of Antarctica. Hydrobiologia 85: 3–15.

    Article  Google Scholar 

  • Convey, P., 1996. The influence of environmental characteristics on the life history attributes of Antarctic terrestrial biota. Biological Reviews 71: 191–225.

    Article  Google Scholar 

  • Convey, P., 2013. Antarctic ecosystems. In: Levin, S. A. (ed.) Encyclopedia of Biodiversity, Vol. 1, 2nd edition. Elsevier, San Diego: 179–188.

  • Convey, P. & S. J. McInnes, 2005. Exceptional, tardigrade dominated, ecosystems from Ellsworth Land, Antarctica. Ecology 86: 519–527.

    Article  Google Scholar 

  • Convey, P. & M. I. Stevens, 2007. Antarctic Biodiversity. Science 317: 1877–1878.

    CAS  PubMed  Article  Google Scholar 

  • Convey, P., J. Gibson, C.-D. Hillenbrand, D. A. Hodgson, P. J. A. Pugh, J. L. Smellie & M. I. Stevens, 2008. Antarctic terrestrial life – challenging the history of the frozen continent? Biological Reviews 83: 103–117.

    PubMed  Article  Google Scholar 

  • Convey, P., D. K. A. Barnes, H. Griffiths, S. Grant, K. Linse & D. N. Thomas, 2012. Biogeography and regional classifications of Antarctica. In Rogers, A. D., N. M. Johnston, E. Murphy & A. Clarke (eds), Antarctica: An Extreme Environment in a Changing World, Chapter 15. Blackwell, Oxford: 471–491.

    Google Scholar 

  • Convey, P., S. L. Chown, A. Clarke, D. K. A. Barnes, V. Cummings, H. Ducklow, F. Frati, T. G. A. Green, S. Gordon, H. Griffiths, C. Howard-Williams, A. H. L. Huiskes, J. Laybourn-Parry, B. Lyons, A. McMinn, L. S. Peck, A. Quesada, S. Schiaparelli & D. Wall, 2014. The spatial structure of Antarctic biodiversity. Ecological Monographs 84: 203–244.

    Article  Google Scholar 

  • Courtright, E. M., D. H. Wall & R. A. Virginia, 2001. Determining habitat suitability for soil invertebrates in an extreme environment: the McMurdo Dry Valleys, Antarctica. Antarctic Science 13: 9–17.

    Article  Google Scholar 

  • Crawley, M., 2007. The R Book. Wiley, Chichester.

    Book  Google Scholar 

  • Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Dartnall, H. J. G., 1983. Rotifers of the Antarctic and Subantarctic. Hydrobiologia 104: 57–60.

    Article  Google Scholar 

  • Dartnall, H. J. G., 1992. The reproductive strategies of two Antartic rotifers. Journal of Zoology Zoological Society of London 227: 145–162.

    Article  Google Scholar 

  • Dartnall, H. J. G., 1995a. The rotifers of Heard Island: preliminary survey, with notes on other freshwater groups. Papers and Proceedings of the Royal of Tasmania 129: 7–15.

    Google Scholar 

  • Dartnall, H. J. G., 1995b. Rotifers, and other aquatic invertebrates, from the Larsemann Hills, Antarctica. Papers and Proceedings of the Royal Society of Tasmania 129: 17–23.

    Google Scholar 

  • Dartnall, H. J. G. & E. D. Hollowday, 1985. Antarctic rotifers. British Antarctic Survey Reports 100: 1–46.

    Google Scholar 

  • Davis, R. C., 1981. Structure and function of two Antarctic terrestrial moss communities. Ecological Monographs 51: 125–143.

    Article  Google Scholar 

  • de Beauchamp, P., 1913. Rotifères. Deuxième Expédition Antartique Française, 1908–1910. Maison et Co, Paris: 105-116.

  • de Beauchamp, P., 1940. Turbellariés et Rotifères. In Jeannel, R. (ed.), Croisière du Bougainville aux Iles Australes Françaises. Mémoires du Muséum National d’Histoire Naturelle, Nouvelle Série 14: 313–326.

  • De Smet, W. H., 1998. Preparation of rotifer trophi for light and scanning electronic microscopy. Hydrobiologia 387(883): 117–121.

    Article  Google Scholar 

  • De Smet, W. H. & E. A. Van Rompu, 1994. Rotifera and Tardigrada from some cryoconite holes of a Spitsbergen (Svalbard) glacier. Belgian Journal of Zoology 124: 27.

    Google Scholar 

  • De Wever, A., F. Leliaert, E. Verleyen, P. Vanormelingen, K. Van der Gucht, D. A. Hodgson, K. Sabbe & W. Vyverman, 2009. Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proceedings of the Royal Society B 276: 3591–3599.

    PubMed Central  PubMed  Article  Google Scholar 

  • Donner, J., 1965. Ordnung Bdelloidea. (Rotatoria, Rädertiere). Bestimmungsbücher zur Bodenfauna Europas 6. Akademie Verlag, Berlin.

  • Donner, J., 1972a. Bericht über Funde von Rädertieren (Rotatoria) aus der Antarctis. Polskie Archiwum Hydrobiologii 19: 251–252.

    Google Scholar 

  • Donner, J., 1972b. Die Rädertierbestände submerser Moose und weiterer Merotope im Bereich der Stauräume der Donau an der deutch-österreichischen Landesgrenze. Archiv für Hydrobiologie Suppl 44: 49–114.

    Google Scholar 

  • Donner, J., 1980. Einige neue Forschungen über bdelloide Rotatorien, besonders in Böden. Revue d’Ecologie et de Biologie du Sol 17: 125–143.

    Google Scholar 

  • Dougherty, E. C., 1964. Cultivation and nutrition of micrometazoa: I. The Antarctic rotifer Philodina gregaria Murray, 1910. Transactions of American Microscopical Society 53: 1–8.

    Article  Google Scholar 

  • Dougherty, E. C. & L. G. Harris, 1963. Antarctic Micrometazoa: fresh-water species in the McMurdo Sound Area. Science 140: 497–498.

    CAS  PubMed  Article  Google Scholar 

  • Dumont, H. J., 1983. Biogeography of rotifers. Hydrobiologia 104: 19–30.

    Article  Google Scholar 

  • Everitt, D. A., 1981. An ecological study of an Antarctic freshwater pool with particular reference to Tardigrada and Rotifera. Hydrobiologia 83: 225–237.

    Article  Google Scholar 

  • Fenchel, T. & B. J. Finlay, 2004. The ubiquity of small species: patterns of local and global diversity. BioScience 54: 777–784.

    Article  Google Scholar 

  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. C. Vrijenhoek, 1994. DNA primers for amplifcation of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    CAS  PubMed  Google Scholar 

  • Fontaneto, D., E. A. Herniou, C. Boschetti, M. Caprioli, G. Melone, C. Ricci & T. G. Barraclough, 2007. Independently evolving species in asexual bdelloid rotifers. PLoS Biology 5: 914–921.

    CAS  Article  Google Scholar 

  • Fontaneto, D., T. G. Barraclough, K. Chen, C. Ricci & E. A. Herniou, 2008. Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Molecular Ecology 17: 3136–3146.

    CAS  PubMed  Article  Google Scholar 

  • Fontaneto, D., C. Q. Tang, U. Obertegger, F. Leasi & T. G. Barraclough, 2012. Different diversification rates between sexual and asexual organisms. Journal of Evolutionary Biology 39: 262–270.

    Article  Google Scholar 

  • Fontaneto, D., N. Iakovenko & W. De Smet, 2015. Diversity gradients of rotifer species richness in Antarctica. Hydrobiologia. doi:10.1007/s10750-015-2258-5.

    Google Scholar 

  • Fraser, C. I., A. Terauds, J. Smellie, P. Convey & S. L. Chown, 2014. Geothermal activity helps life survive ice ages. Proceedings of the National Academy of Sciences of the USA 111: 5634–5639.

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Freckman, D. W. & R. A. Virginia, 1993. Extraction of nematodes from Dry Valley Antarctic soils. Polar Biology 13: 483-487.

    Article  Google Scholar 

  • Fujisawa, T. & T. G. Barraclough, 2013. Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62: 707–724.

    PubMed Central  PubMed  Article  Google Scholar 

  • Ganter, P. F., 2011. Everything is not everywhere: the distribution of cactophilic yeast. In Fontaneto, D. (ed.), Biogeography of microscopic organisms. Cambridge University Press, Cambridge: 130–174.

    Chapter  Google Scholar 

  • Garey, J. R., S. J. McInnes & P. B. Nichols, 2008. Global diversity of tardigrades (Tardigrada) in freshwater. Hydrobiologia 595: 101–106.

    Article  Google Scholar 

  • Greenslade, P., 1995. Collembola from the Scotia Arc and Antarctic Peninsula including descriptions of two new species and notes on biogeography. Polskie Pismo Entomologiczne 64: 305–319.

    Google Scholar 

  • Haigh, S. B., 1965. The bdelloid rotifers of New Zealand, part II. Journal of the Quekett Microscopical Club 30(7–13): 36–41.

    Google Scholar 

  • Haigh, S. B., 1966. The bdelloid rotifers of New Zealand, Part III. Journal of the Quekett Microscopical Club 30: 193–201.

    Google Scholar 

  • Hillebrand, H. & A. I. Azovsky, 2001. Body size determines the strength of the latitudinal diversity gradient. Ecography 24: 251–256.

    Article  Google Scholar 

  • Martiny, J. B. H., B. J. Bohannan, J. H. Brown, R. K. Colwell, J. A. Fuhrman, J. L. Green, M. C. Horner-Devine, M. Kane, J. A. Krumins, C. R. Kuske, P. J. Morin, S. Naeem, L. Øvreås, A.-L. Reysenbach, V. H. Smith & J. T. Staley, 2006. Microbial biogeography: putting microorganisms on the map. Nature Reviews Microbiology 4: 102–112.

    CAS  PubMed  Article  Google Scholar 

  • Iakovenko, N., 2004. Dynamika naselennia kolovertok pidstylky suboru v zymovyy period. In Ivanets, O. R. (ed.), Naukovi osnovy zberezennia biotychnoi riznomanitnosti. Tematychnyi zbirnyk v. 5. Liga-Press, Lviv: 279–284.

    Google Scholar 

  • Iakovenko, N. S. & O. V. Tyshchenko, 2006. Rotifers (Rotifera) as a part of terrestrial bryophytic communities in Argentina Archipelago islands (Antarctic), Russia in the Antarctic. AASRI, St.-Petersburg: 229–230.

    Google Scholar 

  • Iakovenko, N. S., E. Kašparová, M. Plewka & K. Janko, 2013. Otostephanos (Rotifera, Bdelloidea, Habrotrochidae) with the description of two new species. Systematics and Biodiversity 11: 477–494.

    Article  Google Scholar 

  • Jennings, P. G., 1976a. Ecological Studies on Antartic Tardigrades and Rotifers. Ph.D. Thesis, University of Leicester.

  • Jennings, P. G., 1976b. The Tardigrada of Signy Island, South Orkney Islands, with a note on Rotifera. BAS Bulletin 44: 1–25.

    Google Scholar 

  • Jennings, P. G., 1979. The Signy Island terrestrial reference sites: population dynamics of Tardigrada and Rotifera. BAS Bulletin 47: 89–105.

    Google Scholar 

  • Katoh, K., K. Misawa, K. Kuma & T. Miyata, 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066.

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Koste, W., 1996a. Über die moosbewohnende Rotatorienfauna Madagaskars. Osnabrücker Naturwissenschaftliche Mitteilungen 22: 235–253.

    Google Scholar 

  • Koste, W., 1996b. On soil Rotatoria from a lithotelma near Halali Lodge in Etosha National Park in N-Namibia, South Africa. Internationale Revue der gesamten Hydrobiologie und Hydrographie 81: 353–365.

    Article  Google Scholar 

  • Kutikova, L. A., 2005. Bdelloidnye kolovratki fauny Rossii. KMK Press, St. Peterburg.

    Google Scholar 

  • Lacap, D. C., M. C. Y. Lau & S. B. Pointing, 2011. Biogeography of procaryotes. In Fontaneto, D. (ed.), Biogeography of microscopic organisms. Cambridge University Press, Cambridge: 35–42.

    Chapter  Google Scholar 

  • Maslen, N. R. & P. Convey, 2006. Nematode diversity and distribution in the southern maritime Antarctic – clues to history? Soil Biology and Biochemistry 38: 3141–3151.

    CAS  Article  Google Scholar 

  • McGaughran, A., I. D. Hogg & M. I. Stevens, 2008. Patterns of population genetic structure for springtails and mites in southern Victoria Land, Antarctica. Molecular Phylogenetics and Evolution 46: 606–618.

    CAS  PubMed  Article  Google Scholar 

  • McGaughran, A., G. Torricelli, A. Carapelli, F. Frati, M. I. Stevens, P. Convey & I. D. Hogg, 2010. Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica. Journal of Biogeography 37: 103–119.

    Article  Google Scholar 

  • Milne, W., 1916. On the Bdelloid Rotifera of South Africa. Journal of the Quekett Microscopical Club 13(47–83): 149–184.

    Google Scholar 

  • Murray, J., 1910. Antarctic Rotifera. British Antarctic. Expedition 1907–9(1): 41–65.

    Google Scholar 

  • Murray, J., 1911. Bdelloid Rotifera of the South Africa. Annals Mededelingen of the van het Transvaal Museum 3: 1–19.

    Google Scholar 

  • Nkem, J. N., D. N. Wall, R. A. Virginia, J. E. Barrett, E. J. Broos, D. L. Porazinska & B. J. Adams, 2006. Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica. Polar Biology 29: 346–352.

    Article  Google Scholar 

  • Örstan, A., 1992. Toxicity of acrylamide derivatives to embryos of the rotifer Adineta vaga. Bulletin of Environmental Contamination and Toxicology 48: 901–906.

    PubMed  Article  Google Scholar 

  • Örstan, A., 1995. A new species of bdelloid rotifer from Sonora, Mexico. The Southwestern Naturalist 40: 255–258.

    Google Scholar 

  • Peck, L. S., P. Convey & D. K. A. Barnes, 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biological Reviews 81: 75–109.

    PubMed  Article  Google Scholar 

  • Pisa, S., E. M. Biersma, P. Convey, J. Patiño, A. Vanderpoorten, O. Werner & R. M. Ros, 2014. The cosmopolitan moss Bryum argenteum in Antarctica: recent colonization or in situ survival? Polar Biology 37: 1469–1477.

    Article  Google Scholar 

  • Porazinska, D. L., D. H. Wall & R. A. Virginia, 2002. Invertebrates in ornithogenic soils on Ross Island. Antarctica. Polar Biol. 25: 569–574.

    Google Scholar 

  • Porazinska, D. L., A. G. Fountain, T. H. Nylen, M. Tranter, R. A. Virginia & D. H. Wall, 2004. The Biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arctic, Antarctic, and Alpine Research 36: 84–91.

    Article  Google Scholar 

  • Priddle, J. & H. J. G. Dartnall, 1978. The biology of an Antarctic aquatic moss community. Freshwater Biology 8: 469–480.

    Article  Google Scholar 

  • 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: 232–421.

    Article  Google Scholar 

  • Pugh, P. J. A. & P. Convey, 2008. Surviving out in the cold: Antarctic endemic invertebrates and their refugia. Journal of Biogeography 35: 2176–2186.

    Article  Google Scholar 

  • Rambaut, A., 2012. FigTree v.1.4.2. http://tree.bio.ed.ac.uk/software/figtree/.

  • Rambaut, A., M. A. Suchard, W. Xie, A. J. Drummond, 2013. Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer.

  • Ricci, C., 1987. Ecology of bdelloids: how to be successful. Hydrobiologia 147: 117–127.

    Article  Google Scholar 

  • Ricci, C., 2001. Dormancy patterns in rotifers. Hydrobiologia 446(447): 1–11.

    Article  Google Scholar 

  • Ricci, C. & M. Caprioli, 2005. Anhydrobiosis in bdelloid species, populations and individuals. Integrative and Comparative Biology 45: 750–763.

    Article  Google Scholar 

  • Ricci, C., G. Melone & E. Walsh, 2001. A carnivorous bdelloid rotifer, Abrochtha carnivora n. sp. Invertebrate Biology 120: 136–141.

    Article  Google Scholar 

  • Ricci, C., R. Shiel, D. Fontaneto & G. Melone, 2003. Bdelloid Rotifers Recorded from Australia with Description of Philodinavus aussiensis n.sp. Zoologischer Anzeiger 242: 241–248.

    Article  Google Scholar 

  • Richters, F., 1907. Die Fauna der Moosrasen des Gaussbergs und einiger südlicher Inseln. Deutsche Südpolar-Expedition 1901–1903(9): 259–302.

    Google Scholar 

  • Richters, F., 1908. Moosbewohner. Schwedischen Südpolar. Expedition 1901–1903(4): 1–16.

    Google Scholar 

  • Robeson, M. S., A. J. King, K. R. Freeman, C. W. Birky, A. P. Martin & S. K. Schmidt, 2011. Soil rotifer communities are extremely diverse globally but spatially autocorrelated locally. Proceedings of National Academy of Sciences of the United States of America 108: 4406–4410.

    CAS  Article  Google Scholar 

  • Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    PubMed Central  PubMed  Article  Google Scholar 

  • Ruttner-Kolisko, A. & E. Kronsteiner, 1979. Autokologie Parameter von Rotatorien aus extremen Biotopen. Jahresbericht Biologische Station Lunz 2: 111–114.

    Google Scholar 

  • Sanderson, M. J., 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19: 101–109.

    CAS  PubMed  Article  Google Scholar 

  • Segers, H., 2007. Annotated checklist of the rotifers (Phylum Rotifera), with the notes on nomenclature, taxonomy and distribution. Zootaxa 1564: 1–104.

    Google Scholar 

  • Smykla, J., D. L. Porazinska, N. Iakovenko, K. Janko, W. M. Weiner, A. W. Niedbala & M. Drewnik, 2010. Studies on the Antarctic soil invertebrates: preliminary data on rotifers (Rotatoria) with notes on other taxa from Edmonson Point (Northern Victoria Land, Continental Antarctic). Acta Societatis Zoologicae Bohemicae 74: 135–140.

    Google Scholar 

  • Smykla, J., B. Krzewicka, K. Wilk, S. D. Emslie & L. Śliwa, 2011. Additions to the lichen flora of Victoria Land, Antarctica. Polish Polar Research 32: 123–138.

    Article  Google Scholar 

  • Smykla, J., N. Iakovenko, M. Devetter & Ł. Kaczmarek, 2012. Diversity and distribution of tardigrades in soils of Edmonson Point (Northern Victoria Land, continental Antarctica). Czech Polar Reports 2: 61–70.

    Article  Google Scholar 

  • Smykla, J., M. Drewnik, E. Szarek-Gwiazda, Y. S. Hii, W. Knap & S. D. Emslie, 2015. Variation in the characteristics and development of soils at Edmonson Point due to abiotic and biotic factors, northern Victoria Land, Antarctica. Catena 132: 56–67.

    CAS  Article  Google Scholar 

  • Sohlenius, B. & S. Boström, 2005. The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28: 439–448.

    Article  Google Scholar 

  • Sohlenius, B. & S. Boström, 2008. Species diversity and random distribution of microfauna in extremely isolated habitable patches on Antarctic nunataks. Polar Biology 31: 817–825.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stevens, M. I. & I. D. Hogg, 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 and Biochemistry 38: 3171–3180.

    CAS  Article  Google Scholar 

  • Stevens, M. I. S., F. Frati, A. McGaughran, G. Spinsanti & D. Hogg, 2006. Phylogeographic structure suggests multiple glacial refugia in northern Victoria Land for the endemic Antarctic springtail Desoria klovstadi (Collembola, Isotomidae). Zoologica Scripta 36: 201–212.

    Article  Google Scholar 

  • Strunecký, O., J. Elster & J. Komárek, 2012. Molecular clock evidence for survival of Antarctic cyanobacteria (Oscillatoriales, Phormidium autumnale) from Paleozoic times. Microbiol Ecology 82: 482–490.

    Article  CAS  Google Scholar 

  • Sudzuki, M., 1964. On the microfauna of the Antarctic region, I. Moss-water community at Langhovde. Japanese Antarctic Research Expedition Scientific Reports, Series E 19: 1–41.

    Google Scholar 

  • Sudzuki, M., 1979. On the microfauna of the Antarctic region, III. Microbiota of the terrestrial interstices. Memoirs of National Institute of Polar Research (Tokyo). Special issue 11: 104–126.

    Google Scholar 

  • Sudzuki, M., 1988. Comments on the antarctic Rotifera. Hydrobiologia 165: 89–96.

    Article  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Terauds, A., S. L. Chown, F. Morgan, H. J. Peat, D. Watts, H. Keys, P. Convey & D. M. Bergstrom, 2012. Conservation biogeography of the Antarctic. Diversity and Distributions 18: 726–741.

    Article  Google Scholar 

  • Torricelli, G., F. Frati, P. Convey, M. Telford & A. Carapelli, 2010. Population structure of Friesea grisea (Collembola, Neanuridae) in the Antarctic Peninsula and Victoria Land: evidence for local genetic differentiation of pre-Pleistocene origin. Antarctic Science 22: 757–765.

    Article  Google Scholar 

  • Velasco-Castrillón, A. & M. I. Stevens, 2014. Morphological and molecular diversity at a regional scale: a step closer to understanding Antarctic nematode biogeography. Soil Biology and Biochemistry 70: 272–284.

    Article  CAS  Google Scholar 

  • Velasco-Castrillón, A., T. J. Page, J. A. E. Gibson & M. I. Stevens, 2014a. Surprisingly high levels of biodiversity and endemism amongst Antarctic rotifers uncovered with mitochondrial DNA. Biodiversity. doi:10.1080/14888386.2014.930717.

    Google Scholar 

  • Velasco-Castrillón, A., M. B. Schultz, F. Colombo, J. A. E. Gibson, K. A. Davies, A. D. Austin & M. I. Stevens, 2014b. Distribution and diversity of soil microfauna from East Antarctica: assessing the link between biotic and abiotic factors. PLoS One 9: e87529.

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  • Velasco-Castrillón, A., J. A. E. Gibson & M. I. Stevens, 2014c. A review of current Antarctic limno-terrestrial microfauna. Polar Biology 37: 1517–1531.

    Article  Google Scholar 

  • Voigt, M., 1956–1957. Rotatoria: Die Rädertiere Mitteleuropas. Berlin-Nikolassee, Berlin.

  • Vyverman, W., E. Verleyen, A. Wilmotte, D. A. Hodgson, A. Willems, K. Peeters, B. Van de Vijver, A. De Wever, F. Leliaert & K. Sabbe, 2010. Evidence for widespread endemism among Antarctic micro-organisms. Polar Science 4: 103–113.

    Article  Google Scholar 

  • Williams, D. M., 2011. Historical biogeography, microbial endemism and the role of classification: everything is endemic. In Fontaneto, D. (ed.), Biogeography of microscopic organisms. Cambridge University Press, Cambridge: 11–31.

    Chapter  Google Scholar 

  • Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 15: 2869–2876.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Dr. D. Fontaneto, Prof. W. H. De Smet and Prof. L. A. Kutikova for providing a number of poorly accessible literature sources and Dr. Ioanna Vaňková for her kind help and consultations on the Latin names for the new species. Prof. T. G. Barraclough is acknowledged for providing important suggestions on species delimitation methods and the code for PCA. Dr. V. N. Fursov is acknowledged for the help in imaging rotifers. We acknowledge the Centre for Polar Ecology of the University of South Bohemia, Polish Academy of Sciences, National Academy of Sciences of Ukraine, the Academy of Sciences of the Czech Republic, the National Antarctic Scientific Centre of Ukraine and the Centre “Animalia” at the Schmalhausen Institute of Zoology, Kiev, for the financial support and providing equipment and Raytheon Polar Services for logistical support. Funding also was provided by the Polish Ministry of Science and Higher Education (PMSHE) Program for Supporting International Mobility of Scientists and PMSHE grant nos. 2P04F00127, NN304069033 and NN305376438 (JS), the National Science Foundation project no. ANT 0739575 (JS), the Grant Agency of the Czech Academy of Sciences grant no. KJB600450903 (KJ, NI, EK), Czech Ministry of Education project no. LM2010009 (KJ), European Social Fund and the Czech Republic-supported project no. CZ.1.07/2.2.00/28.0190 (KJ), the Institute of Environmental Technologies, Ostrava, CZ.1.05/2.1.00/03.0100 supported by the Research and Development for Innovations Operational Program financed by Structural Funds of European Union and State Budget of the Czech Republic (ZĎ). PC is supported by the Natural Environmental Research Council core funding to the British Antarctic Survey’s core ‘Enviornmental Change and Evolution’ program. This paper contributes to the SCAR ‘State of the Antarctic Ecosystem’ program.

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Correspondence to N. S. Iakovenko.

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Guest editors: Diego Fontaneto & Stefano Schiaparelli / Biology of the Ross Sea and Surrounding Areas in Antarctica

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Iakovenko, N.S., Smykla, J., Convey, P. et al. Antarctic bdelloid rotifers: diversity, endemism and evolution. Hydrobiologia 761, 5–43 (2015). https://doi.org/10.1007/s10750-015-2463-2

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  • DOI: https://doi.org/10.1007/s10750-015-2463-2

Keywords

  • Bdelloidea
  • DNA taxonomy
  • Molecular biogeography
  • 4× rule
  • Generalized mixed Yule coalescent
  • Poisson tree processes