Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
Shopping Cart: ( empty )
You are here: Home > Journals > IS > IS23051
RESEARCH ARTICLE
Contents Vol 38(2)

Sample design in biodiversity studies matters: a fine-scale study of Lawrence’s velvet worm, Peripatopsis lawrencei (Onychophora: Peripatopsidae), reveals hidden diversity

Julian A. Nieto Lawrence https://orcid.org/0000-0002-5982-5803 A and Savel R. Daniels https://orcid.org/0000-0003-2956-3256 A *
+ Author Affiliations
- Author Affiliations

A Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa.

* Correspondence to: srd@sun.ac.za

Handling Editor: Gonzalo Giribet

Invertebrate Systematics 38, IS23051 https://doi.org/10.1071/IS23051
Submitted: 16 October 2023  Accepted: 15 January 2024  Published: 7 February 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

A fine-scale phylogenetic and phylogeographic analysis of Peripatopsis lawrencei s.l. was conducted with both mitochondrial and nuclear DNA sequence data, using both external morphology and scanning electron microscopy of taxonomically important characters. A total of 119 sequences were used for the mitochondrial cytochrome c oxidase subunit I (COI) whereas a single representative specimen from each locality was sequenced for the nuclear 18S rRNA locus. Phylogenetic analyses were conducted on the total COI data set and the combined COI + 18S rRNA data set using a Bayesian analysis and maximum likelihood analyses. For the combined DNA sequence data set, a divergence time estimation was further undertaken in BEAST and specimens placed in a phylogenetic framework including all the described Peripatopsis species from South Africa. In addition, a phylogeographic study was conducted exclusively on P. lawrencei s.s. (clade A) using an analysis of molecular variance and haplotype network. Phylogenetic results indicated that, at the Oubos sample locality, two highly distinct genetic lineages were present (clades A and B), whereas a divergence time estimation suggests a Miocene cladogenesis of the novel Oubos lineage. Marked phylogeographic structure was observed for P. lawrencei s.s. (restricted to clade A) across the distribution range with limited maternal dispersal. Morphologically, the two sympatric lineages at Oubos A and B differed in leg pair number, ventral colour and dorsal scale rank counts, as evident from scanning electron microscopy. Our results support the recognition of a distinct species that occurs in sympatry with P. lawrencei s.s. The new species, P. aereus sp. nov. (clade B) is described and the implication for fine-scale taxonomic studies on saproxylic taxa is discussed.

ZooBank: urn:lsid:zoobank.org:pub:AB6E0BDA-7B5F-4FD3-A863-BA7C814E278C

Keywords: cladogenesis, phylogenetics, phylogeography, saproxylic invertebrates, SEM, sympatry, systematics.

References

Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In ‘Proceedings of the 2nd International Symposium on Information Theory’, 2–8 September 1971, Tsahkadsor, Armenia, USSR. (Eds BN Petrov, F Csaki) pp. 267–281. (Akademia Kiado: Budapest, Hungary)

Barnes A, Daniels SR (2019) On the importance of fine-scale sampling in detecting alpha taxonomic diversity among saproxylic invertebrates: a velvet worm (Onychophora: Opisthopatus amaxhosa) template. Zoologica Scripta 48, 243-262.
| Crossref | Google Scholar |

Barnes A, Daniels SR (2022) Refining species boundaries among velvet worms (Onychophora, Peripatopsidae), with the description of two new species of Opisthopatus from South Africa. Invertebrate Biology 141, e12368.
| Crossref | Google Scholar |

Barnes A, Reiss T, Daniels SR (2020) Systematics of the Peripatopsis clavigera species complex (Onychophora: Peripatopsidae) reveals cryptic cladogenic patterning, with the description of five new species. Invertebrate Systematics 34, 569-590.
| Crossref | Google Scholar |

Clement M, Posada D, Crandall KA (2000) TCS: A computer program to estimate gene genealogies. Molecular Ecology 9, 1657-1659.
| Crossref | Google Scholar | PubMed |

Daniels SR, Ruhberg H (2010) Molecular and morphological variation in a South African velvet worm Peripatopsis moseleyi (Onychophora, Peripatopsidae): evidence for cryptic speciation. Journal of Zoology 282(3), 171-179.
| Crossref | Google Scholar |

Daniels SR, Picker MD, Cowlin RM, Hamer ML (2009) Unravelling evolutionary lineages among South African velvet worms (Onychophora: Peripatopsis) provides evidence for widespread cryptic speciation. Biological Journal of the Linnean Society 97, 200-216.
| Crossref | Google Scholar |

Daniels SR, McDonald DE, Picker MD (2013) Evolutionary insight into the Peripatopsis balfouri sensu lato species complex (Onychophora: Peripatopsidae) reveals novel lineages and zoogeographic patterning. Zoologica Scripta 42, 656-674.
| Crossref | Google Scholar |

Daniels SR, Dambire C, Klaus S, Sharma PP (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.
| Crossref | Google Scholar | PubMed |

Dayrat B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407-415.
| Crossref | Google Scholar |

de Queiroz K (2007) Species concepts and species delimitation. Systematic Biology 56, 879-886.
| Crossref | Google Scholar | PubMed |

Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| Crossref | Google Scholar | PubMed |

Edgecombe GD (2009) Palaeontological and molecular evidence linking Arthropods, Onychophorans, and other Ecdysozoa. Evolution: Education and Outreach 2, 178-190.
| Crossref | Google Scholar |

Excoffier L, Lischer HEL (2010) ARLEQUIN suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564-567.
| Crossref | Google Scholar | PubMed |

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
| Google Scholar | PubMed |

Giribet G, Carranza S, Baguñà J, Riutort M, Ribera C (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76-84.
| Crossref | Google Scholar | PubMed |

Giribet G, Buckman-Young RS, Costa CS, Baker CM, Benavides LR, Branstetter MG, Daniels SR, Pinto-da-Rocha R (2018) The ‘Peripatos’ in Eurogondwana? Lack of evidence that south-east Asian onychophorans walked through Europe. Invertebrate Systematics 32, 842-865.
| Crossref | Google Scholar |

Grobler PCJ, Myburgh AM, Barnes A, Daniels SR (2023) Integrative taxonomy provides evidence for a cryptic lineage in the velvet worm Peripatopsis birgeri species complex (Onychophora: Peripatopsidae) in KwaZulu–Natal, South Africa. Systematics and Biodiversity 21, 2207574.
| Crossref | Google Scholar |

Hamer ML, Samways MJ, Ruhherg H (1997) A review of the Onychophora of South Africa, with discussion of their conservation. Annuals of the Natal Museum 38, 283-312.
| Crossref | Google Scholar |

Heled J, Drummond AJ (2010) Bayesian Inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570-580.
| Crossref | Google Scholar | PubMed |

McDonald DE, Daniels SR (2012) Phylogeography of the Cape velvet worm (Onychophora: Peripatopsis capensis) reveals the impact of Pliocene/Pleistocene climatic oscillations on Afromontane forest in the Western Cape, South Africa. Journal of Evolutionary Biology 25, 824-835.
| Crossref | Google Scholar | PubMed |

McDonald DE, Ruhberg H, Daniels SR (2012) Two new Peripatopsis species (Onychophora: Peripatopsidae) from the Western Cape province, South Africa. Zootaxa 3380, 55-68.
| Crossref | Google Scholar |

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In ‘2010 Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. Accession Number 11705685. (IEEE) 10.1109/GCE.2010.5676129

Mucina LMC, Rutherford R (2006) ‘The Vegetation of South Africa, Lesotho and Swaziland.’ (South African National Biodiversity Institute: Pretoria, South Africa)

Murienne J, Daniels SR, Buckley TR, Mayer G, Giribet G (2014) A living fossil tale of Pangaean biogeography. Proceedings of the Royal Society: Biological Sciences 281, 20132648.
| Crossref | Google Scholar | PubMed |

Myburgh AM, Daniels SR (2015) Exploring the impact of habitat size on phylogeographic patterning in the Overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae). Journal of Heredity 106, 296-305.
| Crossref | Google Scholar | PubMed |

Myburgh AM, Daniels SR (2022) Between the Cape Fold Mountains and the deep blue sea: comparative phylogeography of selected codistributed ectotherms reveals asynchronous cladogenesis. Evolutionary Applications 15, 1967-1987.
| Crossref | Google Scholar | PubMed |

Oliveira IS (2023) An updated world checklist of velvet worms (Onychophora) with notes on nomenclature and status of names. ZooKeys 1184, 133-260.
| Crossref | Google Scholar | PubMed |

Oliveira IS, Lacorte GA, Fonseca CG, Wieloch AH, Mayer G (2011) Cryptic Speciation in Brazilian Epiperipatus (Onychophora: Peripatidae) reveals an underestimated diversity among the peripatid velvet worms. PLoS One 6, e19973.
| Crossref | Google Scholar | PubMed |

Posada D (2008) jModelTest: phylogenetic averaging. Molecular Biology and Evolution 25, 1253-1256.
| Crossref | Google Scholar | PubMed |

Rockman MV, Rowell DM, Tait NN (2001) Phylogenetics of Planipapillus, lawn headed onychophorans of the Australian Alps, based on nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 21, 103-116.
| Crossref | Google Scholar | PubMed |

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Ruhberg H (1985) Die Peripatopsidae (Onychophora). Systematik, Ökologie, Chorologie und phylogenetische Aspekte. Zoologica 137, 1-183.
| Google Scholar |

Ruhberg H, Hamer ML (2005) A new species of Opisthopatus Purcell, 1899 (Onychophora: Peripatopsidae) from KwaZulu–Natal, South Africa. Zootaxa 1039, 27-38.
| Crossref | Google Scholar |

Ruhberg H, Daniels SR (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.
| Crossref | Google Scholar |

Sato S, Buckman-Young RS, Harvey MS, Giribet G (2018) Cryptic speciation in a biodiversity hotspot: multilocus molecular data reveal new velvet worm species from Western Australia (Onychophora: Peripatopsidae: Kumbadjena). Invertebrate Systematics 32, 1249-1264.
| Crossref | Google Scholar |

Sepulchre P, Ramstein G, Fluteau F, Schuster M, Tiercelin JJ, Brunet M (2006) Tectonic uplift and Eastern Africa aridification. Science 313, 1419-1423.
| Crossref | Google Scholar | PubMed |

Sherbon BJ, Walker MH (2004) A new species of Peripatopsis from South Africa, P. stelliporata, with observations on embryonic development and sperm degradation (Onychophora, Peripatopsidae). Journal of Zoology London 264, 295-305.
| Crossref | Google Scholar |

Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114-1116.
| Crossref | Google Scholar |

Siesser WG (1980) Late Miocene origin of the Benguela upswelling system off northern Namibia. Science 208, 283-285.
| Crossref | Google Scholar | PubMed |

Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758-771.
| Crossref | Google Scholar | PubMed |

Steinthorsdottir M, Coxall HK, de Boer AM, Huber M, Barbolini N, Bradshaw CD, Burls NJ, Feakins SJ, Gasson E, Henderiks J, Holbourn AE, Kiel S, Kohn MJ, Knorr G, Kürschner WM, Lear CH, Liebrand D, Lunt DJ, Mörs T, Pearson PN, Pound MJ, Stoll H, Strömberg CAE (2021) The Miocene: The future of the past. Paleoceanography and Paleoclimatology 36, e2020PA004037.
| Crossref | Google Scholar |

Swofford D (2002). ‘PAUP* Phylogenetic Analysis using Parsimony (and other methods). Version 4.10.’ (Illinois Natural History Survey: Champaign, IL, USA)

Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564-577.
| Crossref | Google Scholar | PubMed |

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882.
| Crossref | Google Scholar | PubMed |

Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, 232-235.
| Crossref | Google Scholar | PubMed |

Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869-2876.
| Crossref | Google Scholar | PubMed |