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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Revision of Tasmanian viviparous velvet worms (Onychophora : Peripatopsidae) with descriptions of two new species

Ivo de Sena Oliveira A B E , Hilke Ruhberg C , David M. Rowell D and Georg Mayer A
+ Author Affiliations
- Author Affiliations

A Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34312 Kassel, Germany.

B Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-901 Belo Horizonte, Brazil.

C Center of Natural History (CeNak), University of Hamburg, Zoological Museum, Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany.

D Division of Ecology and Evolution, Research School of Biology, Australian National University, 2601, Canberra, ACT, Australia.

E Corresponding author. Email: ivo.oliveira@uni-kassel.de

Invertebrate Systematics 32(4) 909-932 https://doi.org/10.1071/IS17096
Submitted: 16 December 2017  Accepted: 19 February 2018   Published: 16 August 2018

Abstract

The restricted distribution of viviparous onychophorans in Tasmania has long been a subject of discussion, but their evolutionary history remains unclear. We applied morphological, molecular and karyological methods to assess the taxonomy and phylogenetic relationships of the four viviparous species reported from Tasmania, including Tasmanipatus barretti, T. anophthalmus and two undescribed species previously referred to as ‘Tasmania’ sp. 1 and sp. 2. We demonstrate that all four species can be unambiguously distinguished based on independent character sets. The two ‘Tasmania’ species, which were previously thought to be cryptic, proved to exhibit a set of distinct morphological characters. Molecular phylogenetic analyses revealed that the four species belong to a major clade that includes Peripatoides from New Zealand, and that species from the two landmasses show reciprocal monophyly within this clade. Within the Tasmanian clade, T. anophthalmus is more closely related to the two ‘Tasmania’ species than to T. barretti. Based on this relationship and the lack of morphological and/or karyological characters supporting the Tasmanian viviparous clade, we erect two new genera to accommodate the two ‘Tasmania’ species (Diemenipatus, gen. nov.) and T. anophthalmus (Leucopatus, gen. nov.). An emended diagnosis followed by a redescription of T. barretti is provided and ‘Tasmania’ sp. 1 and sp. 2 are formally described as D. taiti, gen. et sp. nov. and D. mesibovi, gen. et sp. nov., respectively.

Additional keywords: Australia, biodiversity, molecular systematics, taxonomy.


References

Abascal, F., Zardoya, R., and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.
ProtTest: selection of best-fit models of protein evolution.Crossref | GoogleScholarGoogle Scholar |

Abascal, F., Zardoya, R., and Telford, M. J. (2010). TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38, W7–W13.
TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations.Crossref | GoogleScholarGoogle Scholar |

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In ‘Second International Symposium on Information Theory’. (Eds B. N. Petrov and F. Csaki.) pp. 267–281. (Akademiai Kiado: Japan.)

Allwood, J., Gleeson, D., Mayer, G., Daniels, S. R., Beggs, J. R., and Buckley, T. R. (2010). Support for vicariant origins of the New Zealand Onychophora. Journal of Biogeography 37, 669–681.
Support for vicariant origins of the New Zealand Onychophora.Crossref | GoogleScholarGoogle Scholar |

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar |

Anonymous (1990). Fauna. In ‘Tasmania’s World Heritage Area’. p. 5. (Department of Parks, Wildlife and Heritage: Hobart, Tasmania.)

Baehr, M. (1977). Über einige Onychophoren aus Australien und Tasmanien mit Beschreibung einer neuen Art und Anmerkung zur Stellung von Ooperipatus paradoxus Bouvier, 1915. Zoologische Jahrbucher. Abteilung fur Systematik, Geographie und Biologie der Tiere 104, 9–19.

Baer, A., and Mayer, G. (2012). Comparative anatomy of slime glands in Onychophora (velvet worms). Journal of Morphology 273, 1079–1088.
Comparative anatomy of slime glands in Onychophora (velvet worms).Crossref | GoogleScholarGoogle Scholar |

Baer, A., Oliveira, I. S., Steinhagen, M., Beck-Sickinger, A. G., and Mayer, G. (2014). Slime protein profiling: a non-invasive tool for species identification in Onychophora (velvet worms). Journal of Zoological Systematics and Evolutionary Research 52, 265–272.
Slime protein profiling: a non-invasive tool for species identification in Onychophora (velvet worms).Crossref | GoogleScholarGoogle Scholar |

Barrett, C. (1938). A note on Peripatus. Victorian Naturalist 55, 11–12.

Bouvier, E. L. (1905). Monographie des Onychophores. Annales des Sciences Naturelles Zoologie et Biologie Animale [9e Série] 2, 1–383.

Bouvier, E. L. (1907). Monographie des Onychophores. Annales des Sciences Naturelles Zoologie et Biologie Animale [9e Série] 5, 61–318.

Briscoe, D. A., and Tait, N. N. (1993). Peripatus or velvet worms. In ‘Tasmanian Wilderness. World Heritage Values’. (Eds S. Smith and L. Gilfedder.) pp. 136–138. (Royal Society of Tasmania: Hobart, Tasmania.)

Brockmann, C. (2007). Die oviparen Peripatopsidae Tasmaniens (Onychophora): Revision von Ooperipatellus und Bemerkungen zur Phylogenie. Universität Hamburg, Hamburg. Available at: http://ediss.sub.uni-hamburg.de/volltexte/2008/3670/ [accessed 18 June 2018]

Cockerell, T. D. A. (1913). Ooperipatus spenceri, nom. nov. Proceedings of the Biological Society of Washington 26, 19.

Daniels, S. R., McDonald, D. E., and Picker, M. D. (2013). Evolutionary insight into the Peripatopsis balfouri sensu lato species complex (Onychophora: Peripatopsidae) reveals novel lineages and zoogeographic patterning. Zoologica Scripta 42, 656–674.
Evolutionary insight into the Peripatopsis balfouri sensu lato species complex (Onychophora: Peripatopsidae) reveals novel lineages and zoogeographic patterning.Crossref | GoogleScholarGoogle Scholar |

Daniels, S. R., Dambire, C., Klaus, S., and Sharma, P. P. (2016). Unmasking alpha diversity, cladogenesis and biogeographical patterning in an ancient panarthropod lineage (Onychophora: Peripatopsidae: Opisthopatus cinctipes) with the description of five novel species. Cladistics 32, 506–537.
Unmasking alpha diversity, cladogenesis and biogeographical patterning in an ancient panarthropod lineage (Onychophora: Peripatopsidae: Opisthopatus cinctipes) with the description of five novel species.Crossref | GoogleScholarGoogle Scholar |

Daniels, S. R., Dreyer, M., and Sharma, P. P. (2017). Contrasting the population genetic structure of two velvet worm taxa (Onychophora: Peripatopsidae: Peripatopsis) in forest fragments along the south-eastern Cape, South Africa. Invertebrate Systematics 31, 781–796.
Contrasting the population genetic structure of two velvet worm taxa (Onychophora: Peripatopsidae: Peripatopsis) in forest fragments along the south-eastern Cape, South Africa.Crossref | GoogleScholarGoogle Scholar |

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |

Fletcher, J. J. (1890). Additional notes on Peripatus leuckarti. Proceedings of the Linnean Society of New South Wales, 2nd Series 5, 469–486.

Gleeson, D. M., Rowell, D. M., Briscoe, A. V., Tait, N. N., and Higgins, A. V. (1998). Phylogenetic relationships among Onychophora from Australasia inferred from the mitochondrial cytochrome oxidase subunit I gene. Molecular Phylogenetics and Evolution 10, 237–248.
Phylogenetic relationships among Onychophora from Australasia inferred from the mitochondrial cytochrome oxidase subunit I gene.Crossref | GoogleScholarGoogle Scholar |

Jeffery, N. W., Oliveira, I. S., Gregory, T. R., Rowell, D. M., and Mayer, G. (2012). Genome size and chromosome number in velvet worms (Onychophora). Genetica 140, 497–504.
Genome size and chromosome number in velvet worms (Onychophora).Crossref | GoogleScholarGoogle Scholar |

Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.
MAFFT version 5: improvement in accuracy of multiple sequence alignment.Crossref | GoogleScholarGoogle Scholar |

Kircher, M., Sawyer, S., and Meyer, M. (2012). Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Research 40, e3.
Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform.Crossref | GoogleScholarGoogle Scholar |

Mayer, G., Franke, F. A., Treffkorn, S., Gross, V., and Oliveira, I. S. (2015). Onychophora. In ‘Evolutionary Developmental Biology of Invertebrates. Vol. 3’. (Ed. A. Wanninger.) pp. 53–98. (Springer: Berlin.)

Mesibov, B. (1990). Velvet worms: a special case of invertebrate fauna conservation. Tasforests 2, 53–56.

Mesibov, R., and Ruhberg, H. (1991). Ecology and conservation of Tasmanipatus barretti and T. anopthalmus, parapatric onychophorans (Onychophora: Peripatopsidae) from Northeastern Tasmania. Papers and Proceedings of the Royal Society of Tasmania 125, 11–16.

Meyer, M., and Kircher, M. (2010). Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols 2010, 1–7.
Illumina sequencing library preparation for highly multiplexed target capture and sequencing.Crossref | GoogleScholarGoogle Scholar |

Montgomery, T. H. (1900). The spermatogenesis of Peripatus (Peripatopsis) balfouri up to the formation of the spermatid. Zoologische Jahrbucher. Abteilung fur Anatomie und Ontogenie der Tiere 14, 277–368.

Murienne, J., Daniels, S. R., Buckley, T. R., Mayer, G., and Giribet, G. (2013). A living fossil tale of Pangean biogeography. Proceedings. Biological Sciences 281, 20132648.
A living fossil tale of Pangean biogeography.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., and Mayer, G. (2013). Apodemes associated with limbs support serial homology of claws and jaws in Onychophora (velvet worms). Journal of Morphology 274, 1180–1190.
Apodemes associated with limbs support serial homology of claws and jaws in Onychophora (velvet worms).Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., and Mayer, G. (2017). A new giant egg-laying onychophoran (Peripatopsidae) reveals evolutionary and biogeographical aspects of Australian velvet worms. Organisms, Diversity & Evolution 17, 375–391.
A new giant egg-laying onychophoran (Peripatopsidae) reveals evolutionary and biogeographical aspects of Australian velvet worms.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., Wieloch, A. H., and Mayer, G. (2010). Revised taxonomy and redescription of two species of the Peripatidae (Onychophora) from Brazil: a step towards consistent terminology of morphological characters. Zootaxa 2493, 16–34.

Oliveira, I. S., Read, V. M. S. J., and Mayer, G. (2012a). A world checklist of Onychophora (velvet worms), with notes on nomenclature and status of names. ZooKeys 211, 1–70.
A world checklist of Onychophora (velvet worms), with notes on nomenclature and status of names.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., Franke, F. A., Hering, L., Schaffer, S., Rowell, D. M., Weck-Heimann, A., Monge-Nájera, J., Morera-Brenes, B., and Mayer, G. (2012b). Unexplored character diversity in Onychophora (velvet worms): a comparative study of three peripatid species. PLoS One 7, e51220.
Unexplored character diversity in Onychophora (velvet worms): a comparative study of three peripatid species.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., Schaffer, S., Kvartalnov, P. V., Galoyan, E. A., Palko, I. V., Weck-Heimann, A., Geissler, P., Ruhberg, H., and Mayer, G. (2013). A new species of Eoperipatus (Onychophora) from Vietnam reveals novel morphological characters for the South-East Asian Peripatidae. Zoologischer Anzeiger 252, 495–510.
A new species of Eoperipatus (Onychophora) from Vietnam reveals novel morphological characters for the South-East Asian Peripatidae.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., Lacorte, G. A., Weck-Heimann, A., Cordeiro, L. M., Wieloch, A. H., and Mayer, G. (2015). A new and critically endangered species and genus of Onychophora (Peripatidae) from the Brazilian savannah – a vulnerable biodiversity hotspot. Systematics and Biodiversity 13, 211–233.
A new and critically endangered species and genus of Onychophora (Peripatidae) from the Brazilian savannah – a vulnerable biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |

Oliveira, I. S., Bai, M., Jahn, H., Gross, V., Martin, C., Hammel, J. U., Zhang, W., and Mayer, G. (2016). Earliest onychophoran in amber reveals Gondwanan migration patterns. Current Biology 26, 2594–2601.
Earliest onychophoran in amber reveals Gondwanan migration patterns.Crossref | GoogleScholarGoogle Scholar |

Pocock, R. I. (1894). Contributions to our knowledge of the arthropod fauna of the West Indies – Part III. Diplopoda and Malacopoda, with a supplement on the Arachnida of the class Pedipalpi. Journal of the Linnean Society of London, Zoology 24, 473–544.
Contributions to our knowledge of the arthropod fauna of the West Indies – Part III. Diplopoda and Malacopoda, with a supplement on the Arachnida of the class Pedipalpi.Crossref | GoogleScholarGoogle Scholar |

Reid, A. L. (1996). Review of the Peripatopsidae (Onychophora) in Australia, with comments on peripatopsid relationships. Invertebrate Taxonomy 10, 663–936.
Review of the Peripatopsidae (Onychophora) in Australia, with comments on peripatopsid relationships.Crossref | GoogleScholarGoogle Scholar |

Reid, A. L. (2000). Descriptions of Lathropatus nemorum, gen. et sp. nov., and six new Ooperipatus Dendy (Onychophora: Peripatopsidae) from south-eastern Australia. Proceedings of the Royal Society of Victoria 112, 153–184.

Robson, E. A., Lockwood, A. P. M., and Ralph, R. (1966). Composition of the blood in Onychophora. Nature 209, 533.
Composition of the blood in Onychophora.Crossref | GoogleScholarGoogle Scholar |

Rockman, M. V., and Rowell, D. M. (2002). Episodic chromosomal evolution in Planipapillus (Onychophora: Peripatopsidae): a phylogenetic approach to evolutionary dynamics and speciation. Evolution 56, 58–69.
Episodic chromosomal evolution in Planipapillus (Onychophora: Peripatopsidae): a phylogenetic approach to evolutionary dynamics and speciation.Crossref | GoogleScholarGoogle Scholar |

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 |

Rowell, D. M., Higgins, A. V., Briscoe, A. V., and Tait, N. N. (1995). The use of chromosomal data in the systematics of viviparous onychophorans from Australia (Onychophora: Peripatopsidae). Zoological Journal of the Linnean Society 114, 139–153.
The use of chromosomal data in the systematics of viviparous onychophorans from Australia (Onychophora: Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |

Rowell, D. M., Rockman, M. V., and Tait, N. N. (2002). Extensive Robertsonian rearrangement: implications for the radiation and biogeography of Planipapillus Reid (Onychophora: Peripatopsidae). Journal of Zoology 257, 171–179.
Extensive Robertsonian rearrangement: implications for the radiation and biogeography of Planipapillus Reid (Onychophora: Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |

Rowell, D. M., Lim, S. L., and Grutzner, F. (2011). Chromosome analysis in invertebrates and vertebrates In ‘Molecular Methods for Evolutionary Genetics. Vol. 772’. (Eds V. Orgogozo and M. V. Rockman.) pp. 13–35. (Humana Press: New York, NY, USA.)

Ruhberg, H. (1985). Die Peripatopsidae (Onychophora). Systematik, Ökologie, Chorologie und phylogenetische Aspekte. Zoologica (Stuttgart) 137, 1–183.

Ruhberg, H., and Daniels, S. R. (2013). Morphological assessment supports the recognition of four novel species in the widely distributed velvet worm Peripatopsis moseleyi sensu lato (Onychophora: Peripatopsidae). Invertebrate Systematics 27, 131–145.
Morphological assessment supports the recognition of four novel species in the widely distributed velvet worm Peripatopsis moseleyi sensu lato (Onychophora: Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |

Ruhberg, H., Mesibov, R., Briscoe, D. A., and Tait, N. N. (1991). Tasmanipatus barretti gen. nov., sp. nov. and T. anophthalmus sp. nov.: two new and unusual onychophorans (Onychophora: Peripatopsidae) from northeastern Tasmania. Papers and Proceedings of the Royal Society of Tasmania 125, 7–10.

Ruhberg, H., Tiemann, H., Mette, A., and Rhode, B. (2001). Evolutionäre Aspekte der Augen-Rückbildung beim hemiedaphischen Onychophoren Tasmanipatus anophthalmus Ruhberg et al., 1991 (Peripatopsidae). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 98, 31–50.

Sänger, N. K. (1871). Peripatus capensis Sr. and Peripatus leuckartii n. sp. Transactions of the Second Congress of Russian Naturalists in Moscow, 239–262.

Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar |

Sunnucks, P., Curach, N. C., Young, A., French, J., Cameron, R., Briscoe, D. A., and Tait, N. N. (2000). Reproductive biology of the onychophoran Euperipatoides rowelli. Journal of Zoology 250, 447–460.
Reproductive biology of the onychophoran Euperipatoides rowelli.Crossref | GoogleScholarGoogle Scholar |

Tait, N., and Briscoe, D. (1989). Peripatus: up here for thinking? Australian Natural History 22, 572–579.

Tait, N. N., and Briscoe, D. A. (1995). Genetic differentiation within New Zealand Onychophora and their relationships to the Australian fauna. Zoological Journal of the Linnean Society 114, 103–113.
Genetic differentiation within New Zealand Onychophora and their relationships to the Australian fauna.Crossref | GoogleScholarGoogle Scholar |

Tait, N. N., Stutchbury, R. J., and Briscoe, D. A. (1990). Review of the discovery and identification of Onychophora in Australia. Proceedings of the Linnean Society of New South Wales 112, 153–171.

Tait, N. N., Briscoe, D. A., and Rowell, D. M. (1995). Onychophora – ancient and modern radiations. Memoirs of the Association of Australasian Palaeontologists 18, 21–30.

Walker, M. H., and Tait, N. N. (2004). Studies on embryonic development and the reproductive cycle in ovoviviparous Australian Onychophora (Peripatopsidae). Journal of Zoology 264, 333–354.
Studies on embryonic development and the reproductive cycle in ovoviviparous Australian Onychophora (Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |