Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea
Matteo Vecchi A , Michele Cesari A C , Roberto Bertolani A , K. Ingemar Jönsson B , Lorena Rebecchi A and Roberto Guidetti AA Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 213/D, Modena, 41125, Italy.
B School of Education and Environment, Kristianstad University, SE-291 88 Kristianstad, Sweden.
C Corresponding author. Email: michele.cesari@unimore.it
Invertebrate Systematics 30(4) 303-322 https://doi.org/10.1071/IS15033
Submitted: 17 July 2015 Accepted: 18 February 2016 Published: 31 August 2016
Abstract
Tardigrades represent one of the most abundant groups of Antarctic metazoans in terms of abundance and diversity, thanks to their ability to withstand desiccation and freezing; however, their biodiversity is underestimated. Antarctic tardigrades from Dronning Maud Land and Victoria Land were analysed from a morphological point of view with light microscopy and scanning electron microscopy, and from a molecular point of view using two genes (18S, 28S) analysed in Bayesian inference and maximum-likelihood frameworks. In addition, indel-coding datasets were used for the first time to infer tardigrade phylogenies. We also compared Antarctic specimens with those from Italy and Greenland. A combined morphological and molecular analysis led to the identification of two new evolutionary lineages, for which we here erect the new genera Acanthechiniscus, gen. nov. (Echiniscidae, Echiniscoidea) and Mesobiotus, gen. nov. (Macrobiotidae, Macrobiotoidea). Moreover, two species new to science were discovered: Pseudechiniscus titianae, sp. nov. (Echiniscidae : Echiniscoidea) and Mesobiotus hilariae, sp. nov. (Macrobiotidae : Macrobiotoidea). This study highlights the high tardigrade diversity in Antarctica and the importance of an integrated approach in faunal and taxonomic studies.
http://zoobank.org/urn:lsid:zoobank.org:pub:8AAB42BF-B781-4418-A385-DC80C18EC31D
Additional keywords: molecular phylogenetics, nuclear DNA, systematics, Tardigrada, taxonomy.
References
Bartoš, E. (1935). Neue Echiniscus-Arten der nördlichen Slowakei. Zoologischer Anzeiger 111, 139–143.Bertolani, R., Biserov, V., Rebecchi, L., and Cesari, M. (2011a). 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., Rebecchi, L., Giovannini, I., and Cesari, M. (2011b). 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., 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 |
Binda, M. G., and Pilato, G. (2000). Diphascon (Adropion) tricuspidatum, a new species of eutardigrade from Antarctica. Polar Biology 23, 75–76.
| Diphascon (Adropion) tricuspidatum, a new species of eutardigrade from Antarctica.Crossref | GoogleScholarGoogle Scholar |
Binda, M. G., Pilato, G., and Lisi, O. (2005). Remarks on Macrobiotus furciger Murray, 1906 and description of three new species of the furciger group (Eutardigrada, Macrobiotidae). Zootaxa 68, 55–68.
Biserov, V. I. (1990a). On the revision of the genus Macrobiotus. The subgenus Macrobiotus s. str.: a new systematic status of the group hufelandi (Tardigrada, Macrobiotidae). Communication 1. Zoologicheskij Zhurnal 69, 5–17.
Biserov, V. I. (1990b). On the revision of the Macrobiotus genus. The subgenus Macrobiotus s. str. is a new taxonomic status of the hufelandi group (Tardigrada, Macrobiotidae). Communication 2. Zoologicheskij Zhurnal 69, 38–50.
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analyses. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=7270e7b94b46ec4a30ad5328609b8552CAS | 10742046PubMed |
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 | 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 |
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 |
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, Dronning Maud Land (Tardigrada). Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 11, 176–182.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=9d94fe4230b53e1213abb545ddca7e97CAS | 15034147PubMed |
Ehrenberg, C. G. (1853). Diagnoses novarum formarum. Monatsberichte der Königlich preussischen Akademie der Wissenschaften zu Berlin, 526–533.
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 | 21402076PubMed |
Guidetti, R., Peluffo, J. R., Rocha, A. M., Cesari, M., and de Peluffo, M. C. M. (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., Rebecchi, L., Cesari, M., and McInnes, S. J. (2014). Mopsechiniscus franciscae, a new species of a rare genus of Tardigrada from continental Antarctica. Polar Biology 37, 1221–1233.
| Mopsechiniscus franciscae, a new species of a rare genus of Tardigrada from continental Antarctica.Crossref | GoogleScholarGoogle Scholar |
Jørgensen, A., Møbjerg, N., and Kristensen, R. M. (2011). Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) – an investigation of the congruence between molecules and morphology. Journal of Zoological Systematics and Evolutionary Research 49, 6–16.
| Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) – an investigation of the congruence between molecules and morphology.Crossref | GoogleScholarGoogle Scholar |
Kaczmarek, Ł., Goldyn, B., Prokop, Z. M., and Michalczyk, Ł. (2011). New records of Tardigrada from Bulgaria with the description of Macrobiotus binieki sp. nov. (Eutardigrada: Macrobiotidae) and a key to the species of the harmsworthi group. Zootaxa 2781, 29–39.
Kaczmarek, Ł., Janko, K., Smykla, J., and Michalczyk, Ł. (2014). Soil tardigrades from the Antarctic Peninsula with a description of a new species and some remarks on the genus Ramajendas (Eutardigrada: Isohypsibiidae). The Polar Record 50, 176–182.
| Soil tardigrades from the Antarctic Peninsula with a description of a new species and some remarks on the genus Ramajendas (Eutardigrada: Isohypsibiidae).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’. (Ed. R. Bertolani.) Vol 1, pp. 261–335. (Mucchi: Modena.)
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 |
Miller, W. R., Miller, J. D., and Heatwole, H. (1996). Tardigrades of the Australian Antarctic Territories: the Windmill Islands, East Antarctica. Zoological Journal of the Linnean Society 116, 175–184.
| Tardigrades of the Australian Antarctic Territories: the Windmill Islands, East Antarctica.Crossref | GoogleScholarGoogle Scholar |
Møbjerg, N., Halberg, K. A., Jørgensen, A., Persson, D. M., Ramløv, 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 |
Müller, K. (2005). SeqState – primer design and sequence statistics for phylogenetic DNA data sets. Applied Bioinformatics 4, 65–69.
| 16000015PubMed |
Müller, K. (2006). Incorporating information from length-mutational events into phylogenetic analysis. Molecular Phylogenetics and Evolution 38, 667–676.
| Incorporating information from length-mutational events into phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 16129628PubMed |
Murray, J. (1906). The Tardigrada of the Scottish lochs. Transactions of the Royal Society of Edinburgh 41, 677–698.
| The Tardigrada of the Scottish lochs.Crossref | GoogleScholarGoogle Scholar |
Murray, J. (1907a). Arctic Tardigrada collected by Wm. S. Bruce. Transactions of the Royal Society of Edinburgh 45, 669–681.
| Arctic Tardigrada collected by Wm. S. Bruce.Crossref | GoogleScholarGoogle Scholar |
Murray, J. (1907b). Encystment of Tardigrada. Transactions of the Royal Society of Edinburgh 45, 837–854.
| Encystment of Tardigrada.Crossref | GoogleScholarGoogle Scholar |
Pilato, G. (1981). Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia 8, 51–57.
Pilato, G., McInnes, S. J., and Lisi, O. (2012). Hebesuncus mollispinus (Eutardigrada, Hypsibiidae), a new species from maritime Antarctica. Zootaxa 68, 60–68.
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=53928922981f8b5b3119f47393588dfaCAS | 18397919PubMed |
Ramazzotti, G., and Maucci, W. (1983). Il Phylum Tardigrada. III Edizione riveduta e aggiornata. Memorie dell’Istituto Italiano di Idrobiologia Dott. Marco de Marchi. (Istituto Italiano di Idrobiologia)
Rambaut, A., and Drummond, A. J. (2007). Tracer v1.5. Available at: http://beast.bio.ed.ac.uk/Tracer
Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D. L., Darling, A., Höhna, 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 | 22357727PubMed |
Sands, C. J., McInnes, S. J., Marley, N. J., Goodall-Copestake, W. P., Convey, P., and Linse, K. (2008). Phylum Tardigrada: an ‘individual’ approach. Cladistics 24, 861–871.
| Phylum Tardigrada: an ‘individual’ approach.Crossref | GoogleScholarGoogle Scholar |
Sanyal, A. K. (2004). Diversity of Invertebrate Fauna of Schirmacher Oasis, East Ant arctica. Nineteenth Indian Expedition to Antarctica. Scientific Report 17. Department of Ocean Development. Technical Publication. pp. 173–187.
Simmons, M. P., and Ochoterena, H. (2000). Gaps as characters in sequence based phylogenetic analyses. Systematic Biology 49, 369–381.
| Gaps as characters in sequence based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntlKjtg%3D%3D&md5=b52edc76bb51f8feeaa87526853d2757CAS | 12118412PubMed |
Sohlenius, B., and Boström, S. (2005). The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28, 439–448.
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.
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 | 16928733PubMed |
Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RaxML web servers. Systematic Biology 57, 758–771.
| A rapid bootstrap algorithm for the RaxML web servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |
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=2f9d873c81808922c1a4a9825a3ce9adCAS | 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=016319dce18b31e62a9233271491f827CAS |
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 | 21546353PubMed |
Tsujimoto, M., McInnes, S. J., Convey, P., and Imura, S. (2014). Preliminary description of tardigrade species diversity and distribution pattern around coastal Syowa Station and inland Sør Rondane Mountains, Dronning Maud Land, East Antarctica. Polar Biology 37, 1361–1367.
| Preliminary description of tardigrade species diversity and distribution pattern around coastal Syowa Station and inland Sør Rondane Mountains, Dronning Maud Land, East Antarctica.Crossref | GoogleScholarGoogle Scholar |
Tumanov, D. V. (2006). Five new species of the genus Milnesium (Tardigrada, Eutardigrada, Milnesiidae). Zootaxa 1122, 1–23.
Utsugi, K., and Ohyama, Y. (1989). Antarctic Tardigrada. Proceedings of the NIPR Symposium on Polar Biology 2, 190–197.
Utsugi, K., and Ohyama, Y. (1991). Antarctic Tardigrada. II. Molodezhnaya and Mt. Riiser-Larsen Areas. Proceedings of the NIPR Symposium on Polar Biology 4, 161–170.
Velasco-Castrillón, A., Page, T. J., Gibson, J. A., and Stevens, M. I. (2014). 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., McInnes, S., Schultz, M., Arróniz-Crespo, M., D’Haese, C., Gibson, J., Adams, B., Page, T., Austin, A., Coopsr, S., and Stevens, M. (2015). Mitochondrial DNA analyses reveal a widespread tardigrade diversity in Antarctica. Invertebrate Systematics 29, 578–590.
| Mitochondrial DNA analyses reveal a widespread tardigrade diversity in Antarctica.Crossref | GoogleScholarGoogle Scholar |
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). Anhydrobiosis in tardigrades – the last decade. Journal of Insect Physiology 57, 577–583.
| Anhydrobiosis in tardigrades – the last decade.Crossref | GoogleScholarGoogle Scholar | 21440551PubMed |
Zawierucha, K., Kolicka, M., Takeuchi, N., and Kaczmarek, Ł. (2015). What animals can live in cryoconite holes? A faunal review. Journal of Zoology 295, 159–169.
| What animals can live in cryoconite holes? A faunal review.Crossref | GoogleScholarGoogle Scholar |