Mitochondrial DNA analyses reveal widespread tardigrade diversity in Antarctica
Alejandro Velasco-Castrillón A K , Sandra J. McInnes B , Mark B. Schultz C , María Arróniz-Crespo D , Cyrille A. D’Haese E , John A. E. Gibson F , Byron J. Adams G , Timothy J. Page H , Andrew D. Austin A , Steven J. B. Cooper A I and Mark I. Stevens I J
+ Author Affiliations
- Author Affiliations
A Australian Centre for Evolutionary Biology and Biodiversity, School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
B British Antarctic Survey, Madingley Road, Cambridge, Cambridgeshire, CB3 0ET, United Kingdom.
C Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Parkville, Vic. 3010, Australia.
D Bangor University, School of Environment, Natural Resources and Geography, 2nd Floor ECW, Bangor, Gwynedd, LL57 2UW, United Kingdom.
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 Department of Biology, and Evolutionary Ecology Laboratories, Brigham Young University, Provo, UT 84602, USA.
H Australian Rivers Institute, Nathan campus, Griffith University, 170 Kessels Road, Nathan, QLD 4111, Australia.
I South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
J School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, SA 5000, Australia.
K Corresponding author. Email: a.velascocastrillon@gmail.com
Invertebrate Systematics 29(6) 578-590 https://doi.org/10.1071/IS14019
Submitted: 8 April 2015 Accepted: 15 September 2015 Published: 22 December 2015
Abstract
Antarctica contains some of the most challenging environmental conditions on the planet due to freezing temperatures, prolonged winters and lack of liquid water. Whereas 99.7% of Antarctica is permanently covered by ice and snow, some coastal areas and mountain ridges have remained ice-free and are able to sustain populations of microinvertebrates. Tardigrades are one of the more dominant groups of microfauna in soil and limno-terrestrial habitats, but little is known of their diversity and distribution across Antarctica. Here, we examine tardigrades sampled from across an extensive region of continental Antarctica, and analyse and compare their partial mitochondrial cytochrome c oxidase subunit 1 (COI) gene sequences with those from the Antarctic Peninsula, maritime and sub-Antarctica, Tierra del Fuego and other worldwide locations in order to recognise operational taxonomic units (OTUs). From 439 new tardigrade COI sequences, we identified 98 unique haplotypes (85 from Antarctica) belonging to Acutuncus, Diphascon, Echiniscus, Macrobiotus, Milnesium and unidentified Parachela. Operational taxonomic units were delimited by Poisson tree processes and general mixed Yule coalescent methods, resulting in 58 and 55 putative species, respectively. Most tardigrades appear to be locally endemic (i.e. restricted to a single geographic region), but some (e.g. Acutuncus antarcticus (Richters, 1904)) are widespread across continental Antarctica. Our molecular results reveal: (i) greater diversity than has previously been appreciated with distinct OTUs that potentially represent undescribed species, and (ii) a lack of connectivity between most OTUs from continental Antarctica and those from other Antarctic geographical zones.
Additional keywords: biodiversity, biogeography, COI gene, cosmopolitan, endemic, OTUs, refugia, species delimitation, Tardigrada.
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFegurs%3D&md5=170884f43a011be0a2add547ef5e7feeCAS |
Andrássy, I. (1998). Nematodes in the sixth continent. Journal of Nematode Morphlogy and Systematics 1, 107–186.
Ashton, G. V., Stevens, M. I., Hart, M. C., Green, D. H., Burrows, M. T., Cook, E. J., and Willis, K. J. (2008). Mitochondrial DNA reveals multiple northern hemisphere introductions of Caprella mutica (Crustacea, Amphipoda). Molecular Ecology 17, 1293–1303.
| Mitochondrial DNA reveals multiple northern hemisphere introductions of Caprella mutica (Crustacea, Amphipoda).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFShtr8%3D&md5=00c95a8b7cc27ce2ddf49ab32d4aaf40CAS | 18302689PubMed |
Bertolani, R., and Rebecchi, L. (1993). A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica Scripta 22, 127–152.
| A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades.Crossref | GoogleScholarGoogle Scholar |
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.
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 | 24657804PubMed |
Blanco-Bercial, L., Cornils, A., Copley, N., and Bucklin, A. (2014). DNA barcoding of marine copepods: assessment of analytical approaches to species identification. PLoS Currents 1, 6.
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=b502860087af1030afc01ee0f39f979aCAS | 21564727PubMed |
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 | 17553768PubMed |
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=d4a945bcd5155b38567cbb451865a8dcCAS | 17901323PubMed |
Convey, P., Gibson, J. A. 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 | GoogleScholarGoogle Scholar | 18429764PubMed |
Costa, F. O., deWaard, J. R., Boutillier, J., Ratnasingham, S., Dooh, R. T., Hajibabaei, M., and Hebert, P. D. N. (2007). Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.
| Biological identifications through DNA barcodes: the case of the Crustacea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Gqsbo%3D&md5=4bea2bdd63fcab6a32dd5ff128d735f8CAS |
Czechowski, P., Sands, C. J., Adams, B., D’Haese, C., Gibson, J., 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 |
Dastych, H. (1984). The Tardigrada from Antarctic with descriptions of several new species. Acta Zoologica Cracoviensia 27, 377–436.
Dastych, H., and Harris, J. M. (1995). A new species of the genus Macrobiotus from inland nunataks in western Dronning Maud Land, continental Antarctica (Tardigrada). Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 11, 175–182.
Dastych, H., Ryan, G., and Watkins, P. (1990). Notes on Tardigrada from western Dronning Maud Land (Antarctica) with a description of two new species. Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 10, 57–66.
Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Fontaneto, D., Barraclough, T. G., Chen, K., Ricci, C., and Herniou, E. A. (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.
| Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps12qsL4%3D&md5=5b88091bd3ab2589aa321e4f16c4942dCAS | 18522694PubMed |
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 | GoogleScholarGoogle Scholar |
Gibson, J. A., 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 |
Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003a). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 313–321.
| Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=3674f949d3018658729ed40e40c01edcCAS |
Hebert, P. D. N., Ratnasingham, S., and deWaard, J. R. (2003b). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, S96–S99.
| Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Smsbo%3D&md5=ec8f4b97cee943c0a02f56c0dc3c13a3CAS |
Hengherr, S., Reuner, A., Brummer, F., and Schill, R. O. (2010). Ice crystallization and freeze tolerance in embryonic stages of the tardigrade Milnesium tardigradum. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 156, 151–155.
| Ice crystallization and freeze tolerance in embryonic stages of the tardigrade Milnesium tardigradum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7otlGkug%3D%3D&md5=059d74efb52a6cc1d019cd42b442d9d0CAS |
Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=cd4de43d633ceeff10f03392cbc4da97CAS | 11524383PubMed |
Huerta-Cepas, J., Dopazo, J., and Gabaldón, T. (2010). ETE: a python Environment for Tree Exploration. BMC Bioinformatics 11, 24.
| ETE: a python Environment for Tree Exploration.Crossref | GoogleScholarGoogle Scholar | 20070885PubMed |
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 |
Kristensen, R. M. (1987). Generic revision of the Echiniscidae (Heterotardigrada), with a discussion of the origin of the family. In ‘Biology of Tardigrades. Selected Symposia and Monographs UZI’. pp. 261–335.
Marley, N. J., McInnes, S. J., and Sands, C. J. (2011). Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 2819, 51–64.
Marshall, D. J., and Pugh, P. J. A. (1996). Origin of the inland Acari of continental Antarctica, with particular reference to Dronning Maud Land. Zoological Journal of the Linnean Society 118, 101–118.
| Origin of the inland Acari of continental Antarctica, with particular reference to Dronning Maud Land.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 26467614PubMed |
McInnes, S. J. (1995). Taxonomy and ecology of tardigrades from Antarctic lakes. Master’s thesis, Open University.
McInnes, S. J. (2010). Echiniscus corrugicaudatus (Heterotardigrada; Echiniscidae) a new species from Ellsworth Land, Antarctica. Polar Biology 33, 59–70.
| Echiniscus corrugicaudatus (Heterotardigrada; Echiniscidae) a new species from Ellsworth Land, Antarctica.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 |
Michalczyk, Ł., Wełnicz, W., Frohme, M., and Kaczmarek, Ł. (2012). Redescriptions of three Milnesium Doyère, 1840 taxa (Tardigrada: Eutardigrada: Milnesiidae), including the nominal species for the genus. Zootaxa 3154, 1–20.
Miller, W. R., and Heatwole, H. (1995). Tardigrades of the Australian Antarctic territories – the Mawson coast, East Antarctica. Invertebrate Biology 114, 27–38.
| Tardigrades of the Australian Antarctic territories – the Mawson coast, East Antarctica.Crossref | GoogleScholarGoogle Scholar |
Miller, W. R., Heatwole, H., Pidgeon, R. W. J., and Gardiner, G. R. (1994). Tardigrades of the Australian Antarctic territories – the Larsemann Hills, East Antarctica. Transactions of the American Microscopical Society 113, 142–160.
| Tardigrades of the Australian Antarctic territories – the Larsemann Hills, East Antarctica.Crossref | GoogleScholarGoogle Scholar |
Modica, M. V., Puillandre, N., Castelin, M., Zhang, Y., and Holford, M. (2014). A good compromise: rapid and robust species proxies for inventorying biodiversity hotspots using the Terebridae (Gastropoda: Conoidea). PLoS One 9, e102160.
| A good compromise: rapid and robust species proxies for inventorying biodiversity hotspots using the Terebridae (Gastropoda: Conoidea).Crossref | GoogleScholarGoogle Scholar | 25003611PubMed |
Murray, J. (1910). Tardigrada, in J. Murray (ed). British Antarctic Expedition 1907–09. Reports on the Scientific Investigations. Biology, Vol. 1, William Heinemann, pp. 83–187.
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. (1999). Three new species of Diphascon of the pingue group (Eutardigrada, Hypsibiidae) from Antarctica. Polar Biology 21, 335–342.
| Three new species of Diphascon of the pingue group (Eutardigrada, Hypsibiidae) from Antarctica.Crossref | GoogleScholarGoogle Scholar |
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.
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., and Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
| Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar | 16967577PubMed |
Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=718ab7cf5a23f1b7a2bd92c5ee779bcaCAS | 9918953PubMed |
Powers, L. E., Freckman, D. W., and Virginia, R. A. (1995). Spatial distribution of nematodes in polar desert soils of Antarctica. Polar Biology 15, 325–333.
| Spatial distribution of nematodes in polar desert soils of Antarctica.Crossref | GoogleScholarGoogle 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, 323–421.
| A synonymic catalogue of the Acari from Antarctica, the sub-Antarctic islands and the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. (2009a). Tracer. MCMC trace analysis tool. Version 1.5. 2003–2009. Computer program distributed by the authors. Available at: http://beast.bio.ed.ac.uk [Accessed September 2013].
Rambaut, A., and Drummond, A. (2009b). FigTree v1. 3.1. Computer program distributed by the authors. Available at: http://tree.bio.ed.ac.uk/software [Accessed September 2013].
Robeson, M., Costello, E., Freeman, K., Whiting, J., Adams, B., Martin, A., and Schmidt, S. (2009). Environmental DNA sequencing primers for eutardigrades and bdelloid rotifers. BMC Ecology 9, 25.
| Environmental DNA sequencing primers for eutardigrades and bdelloid rotifers.Crossref | GoogleScholarGoogle Scholar | 20003362PubMed |
Sands, C. J., Convey, P., Linse, K., and McInnes, S. J. (2008a). 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 | GoogleScholarGoogle Scholar | 18447908PubMed |
Sands, C. J., McInnes, S. J., Marley, N. J., Goodall-Copestake, W. P., Convey, P., and Linse, K. (2008b). Phylum Tardigrada: an ‘individual’ approach. Cladistics 24, 861–871.
| Phylum Tardigrada: an ‘individual’ approach.Crossref | GoogleScholarGoogle Scholar |
Smykla, J., Iakovenko, N., Devetter, M., and Kaczmarek, Ł. (2012). Diversity and distribution of tardigrades in soils of Edmonson Point (Northern Victoria Land, continental Antarctica). Czech Polar Reports 2, 61–70.
| Diversity and distribution of tardigrades in soils of Edmonson Point (Northern Victoria Land, continental Antarctica).Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Sohlenius, B., and Boström, S. (2008). Species diversity and random distribution of microfauna in extremely isolated habitable patches on Antarctic nunataks. Polar Biology 31, 817–825.
| Species diversity and random distribution of microfauna in extremely isolated habitable patches on Antarctic nunataks.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Soldati, L., Kergoat, G. J., Clamens, A. L., Jourdan, H., Jabbour-Zahab, R., and Condamine, F. L. (2014). Integrative taxonomy of New Caledonian beetles: species delimitation and definition of the Uloma isoceroides species group (Coleoptera, Tenebrionidae, Ulomini), with the description of four new species. ZooKeys 415, 133–167.
| Integrative taxonomy of New Caledonian beetles: species delimitation and definition of the Uloma isoceroides species group (Coleoptera, Tenebrionidae, Ulomini), with the description of four new species.Crossref | GoogleScholarGoogle Scholar | 25009426PubMed |
Srivathsan, A., and Meier, R. (2012). On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics 28, 190–194.
| On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVSgt70%3D&md5=def6ca827e5f2e1189c7bed9d98a77a4CAS | 12919474PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFens7s%3D&md5=ecf469e233e3cb0facf1a4be8d8c1138CAS |
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=96b45ae6911eb64f6f57a49adb576800CAS | 16326749PubMed |
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.
Swofford, D. (2002). ‘PAUP* version 4.0. Phylogenetic Analysis Using Parsimony (and Other Methods).’ (Sinauer Associates: Sunderland, MA.)
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=421e650591d1feaa34697a0db6b94378CAS | 21546353PubMed |
Tumanov, D. V. (2006). Five new species of the genus Milnesium (Tardigrada, Eutardigrada, Milnesiidae). Zootaxa 1122, 1–23.
Velasco-Castrillón, A., and Stevens, M. I. (2014). Morphological and molecular diversity at a regional scale: a step closer to understanding Antarctic nematode biogeography. Soil Biology & Biochemistry 70, 272–284.
| Morphological and molecular diversity at a regional scale: a step closer to understanding Antarctic nematode biogeography.Crossref | GoogleScholarGoogle Scholar |
Velasco-Castrillón, A., Page, T. J., Gibson, J. A. E., and Stevens, M. I. (2014a). Surprisingly high levels of biodiversity and endemism amongst Antarctic rotifers uncovered with mitochondrial DNA. Biodiversity 15, 130–142.
| Surprisingly high levels of biodiversity and endemism amongst Antarctic rotifers uncovered with mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Velasco-Castrillón, A., Schultz, M. B., Colombo, F., Gibson, J. A. E., Davies, K. A., Austin, A. D., and Stevens, M. I. (2014b). Distribution and diversity of soil microfauna from East Antarctica: assessing the link between biotic and abiotic factors. PLoS One 9, e87529.
| Distribution and diversity of soil microfauna from East Antarctica: assessing the link between biotic and abiotic factors.Crossref | GoogleScholarGoogle Scholar | 24498126PubMed |
Vicente, F., Fontoura, P., Cesari, M., Rebecchi, L., Guidetti, R., Serrano, A., and Bertolani, R. (2013). Integrative taxonomy allows the identification of synonymous species and the erection of a new genus of Echiniscidae (Tardigrada, Heterotardigrada). Zootaxa 3613, 557–572.
| Integrative taxonomy allows the identification of synonymous species and the erection of a new genus of Echiniscidae (Tardigrada, Heterotardigrada).Crossref | GoogleScholarGoogle Scholar | 24698838PubMed |
Wełnicz, W., Grohme, M. A., Kaczmarek, Ł., Schill, R. O., and Frohme, M. (2011). ITS‐2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada). Journal of Zoological Systematics and Evolutionary Research 49, 34–39.
| ITS‐2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada).Crossref | GoogleScholarGoogle Scholar |
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=237594892ba48b5fbb2ebd0770baaccbCAS | 23990417PubMed |
