Contrasting the population genetic structure of two velvet worm taxa (Onychophora : Peripatopsidae : Peripatopsis) in forest fragments along the south-eastern Cape, South Africa
Savel R. Daniels A C , Megan Dreyer A and Prashant P. Sharma BA Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, Stellenbosch, 7602, South Africa.
B Department of Zoology, University of Wisconson – Madison, Madison, WI 53706, USA.
C Corresponding author. Email: srd@sun.ac.za
Invertebrate Systematics 31(6) 781-796 https://doi.org/10.1071/IS16085
Submitted: 15 December 2016 Accepted: 11 May 2017 Published: 4 December 2017
Abstract
During the present study, we examined the phylogeography and systematics of two species of velvet worm (Peripatopsis Pocock, 1894) in the forested region of the southern Cape of South Africa. A total of 89 P. moseleyi (Wood-Mason, 1879) and 65 P. sedgwicki (Purcell, 1899) specimens were collected and sequenced for the cytochrome c oxidase subunit I mtDNA (COI). In addition, a single P. sedgwicki specimen per sample locality was sequenced for the 18S rRNA locus. Furthermore, morphological variation among P. sedgwicki sample localities were explored using traditional alpha taxonomic characters. DNA sequence data were subjected to phylogenetic analyses using Bayesian inference and population genetic analyses using haplotype networks and analyses of molecular variance (AMOVAs). Phylogenetic results revealed the presence of four and three clades within P. moseleyi and P. sedgwicki respectively. Haplotype networks were characterised by the absence of shared haplotypes between clades, suggesting genetic isolation, a result corroborated by the AMOVA and highly significant FST values. Specimens from Fort Fordyce Nature Reserve were both genetically and morphologically distinct from the two remaining P. sedgwicki clades. The latter result suggests the presence of a novel lineage nested within P. sedgwicki and suggests that species boundaries within this taxon require re-examination.
Additional keywords: conservation, forest fragmentation, speciation.
References
Avise, J. C., and Ball, R. M. (Eds) (1990). Principles of genealogical concordance in species concepts and biological taxonomy. In ‘Oxford Surveys in Evolutionary Biology. Vol. 7’. (Oxford University Press.)Boyer, S. L., Baker, J. M., and Giribet, G. (2007). Deep genetic divergences in Aoraki denticulata (Arachnida, Opiliones, Cyphophthalmi) a widespread ‘mite harvestman’ defies DNA taxonomy. Molecular Ecology 16, 4999–5016.
| Deep genetic divergences in Aoraki denticulata (Arachnida, Opiliones, Cyphophthalmi) a widespread ‘mite harvestman’ defies DNA taxonomy.Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=9f5fa52c2be09a3ab5e2a128c6c6679eCAS |
Daniels, S. R., and 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, 171–179.
| Molecular and morphological variation in a South African velvet worm, Peripatopsis moseleyi (Onychophora, Peripatopsidae): evidence for cryptic speciation.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Picker, M. D., Cowlin, R. M., and Hamer, M. L. (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.
| Unravelling evolutionary lineages among South African velvet worms (Onychophora: Peripatopsis) provides evidence for widespread cryptic speciation.Crossref | GoogleScholarGoogle Scholar |
Daniels, S. R., Mcdonald, D. E., and Picker, M. (2013). Evolutionary insight into the Peripatopsis balfouri sensu lato species complex (Onychophora: Peripatopsidae) reveals novel lineages and zoogeographic patterning. Zoologica Scripta 42, 656–674.
Daniels, S. R., Dambire, C., Klaus, S., and Sharma, P. P. (2016). Unmasking alpha diversity, cladogenesis and biogeographic patterning in an ancient panarthropod lineage (Onychophora: Peripatopsidae: Opisthopatus cinctipes) with the description of five new species. Cladistics 32, 506–537.
| Unmasking alpha diversity, cladogenesis and biogeographic patterning in an ancient panarthropod lineage (Onychophora: Peripatopsidae: Opisthopatus cinctipes) with the description of five new species.Crossref | GoogleScholarGoogle Scholar |
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=1e151a811e335310e17f8244e6b6ccbaCAS |
de Bivort, B. L., and Giribet, G. (2010). A systematic revision of the South African Pettalidae (Archnida: Opiliones: Cyphophthalmi) based on a combined analysis of discrete and continuous morphological characters with the description of seven new species. Invertebrate Systematics 24, 371–406.
| A systematic revision of the South African Pettalidae (Archnida: Opiliones: Cyphophthalmi) based on a combined analysis of discrete and continuous morphological characters with the description of seven new species.Crossref | GoogleScholarGoogle Scholar |
Eeley, H. A. C., Lawes, M. J., and Piper, S. E. (1999). The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa. Journal of Biogeography 26, 595–617.
| The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–297.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=301bf4945988b7429a8e829133746d39CAS |
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 1:STN:280:DyaK2svns1egtQ%3D%3D&md5=8a87d004cd9548ec59cfcf8f158b8e7bCAS |
Giribet, G., Carranza, S., Baguñà, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
| First molecular evidence for the existence of a Tardigrada + Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVylur8%3D&md5=29371bb78974594dbb4d62c79807fd1bCAS |
Hamer, M. L., Samways, M. J., and Ruhberg, H. (1997). A review of the Onychophora of South Africa, with discussion of their conservation. Annals of the Natal Museum 38, 283–312.
Huntley, B., Midgley, G. F., Barnard, P., and Valdes, P. J. (2014). Suborbital climatic variability and centres of biological diversity in the Cape region of southern Africa. Journal of Biogeography 41, 1338–1351.
| Suborbital climatic variability and centres of biological diversity in the Cape region of southern Africa.Crossref | GoogleScholarGoogle Scholar |
Kotze, D. J., and Samways, M. J. (1999). Invertebrate conservation at the interface between the grassland matrix and natural Afromontane forest fragments. Biodiversity and Conservation 8, 1339–1363.
| Invertebrate conservation at the interface between the grassland matrix and natural Afromontane forest fragments.Crossref | GoogleScholarGoogle Scholar |
Lawes, M. J., Eeley, H. A. C., and Piper, S. E. (2000). The relationship between local and regional diversity of indigenous forest fauna in KwaZulu-Natal Province, South Africa. Biodiversity and Conservation 9, 683–705.
| The relationship between local and regional diversity of indigenous forest fauna in KwaZulu-Natal Province, South Africa.Crossref | GoogleScholarGoogle Scholar |
Lindesay, J. A. (1998). Present climate of southern Africa. In ‘Climates of the Southern Continents: Past, Present and Future’. (Eds J. E. Hobbs, J. A. Lindesay and H. A. Bridgman.) pp. 5–62. (John Wiley and Sons: New York.)
McDonald, D. E., and Daniels, S. R. (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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vmtlCntA%3D%3D&md5=159c807bac508f8700888d84b305917dCAS |
Mucina, L., and Geldenhuys, C. J. (2006). Afrotemperate, subtropical and azonal forests. In ‘The Vegetation of South Africa, Lesotho and Swaziland’. (Eds L. Mucina and M. C. Rutherford.) pp. 586–655. (South African National Biodiversity Institute: Pretoria, South Africa.)
Mucina, L. M .C., and Rutherford, R. (2006). The Vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, Pretoria.
Myburgh, A. M., and Daniels, S. R. (2015). Exploring the impact of habitat size on phylogeographic patterning in the Overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae). The Journal of Heredity 106, 296–305.
| Exploring the impact of habitat size on phylogeographic patterning in the Overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |
Nylander, J. A. A., Wilgenbusch, J. C., Warren, D. L., and Swofford, D. L. (2008). AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24, 581–583.
| AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVKis7g%3D&md5=ad936342b4d673bff991203320a25859CAS |
Partridge, T. C., and Maud, R. R. (2000). Macro-scale geomorphic evolution of southern Africa. In ‘The Cenozoic of Southern Africa’. (Eds T. C. Partridge and R. R. Maud.) pp. 3–19. (Oxford University Press: Oxford.)
Reid, N. M., and Carstens, B. C. (2012). Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology 12, 196.
| Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model.Crossref | GoogleScholarGoogle Scholar |
Rockman, M. W., Rowell, D. M., and Tait, N. N. (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.
| 1:CAS:528:DC%2BD3MXnsFOjtb8%3D&md5=7a727f0d26c3c3ad8ad3802fbcd72f86CAS |
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Hohna, 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 |
Ruhberg, H., and Daniels, S. R. (2013). Morphological assessment supports the recognition of four novel species in a 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 a widely-distributed velvet worm Peripatopsis moseleyi sensu lato (Onychophora: Peripatopsidae).Crossref | GoogleScholarGoogle Scholar |
Schneider, S., Roessli, D., and Excoffier, L. (2000). ‘ARLEQUIN Version 2000: Software for Population Genetics Data Analysis.’ (University of Geneva: Switzerland.)
Swofford, D. L. (2002). ‘PAUP* Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4.10.’ (Sinauer Associates: Sunderland, MA.)
Templeton, A. R., Crandall, K. A., and Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
| 1:CAS:528:DyaK3sXhslSrsQ%3D%3D&md5=73e9441bf90c5cdd9b72a6fd95d209f8CAS |
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analyses tools. Nucleic Acids Research 25, 4876–4882.
| The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analyses tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=6ec6dd0c0d4b7f2392408a7bb3c06f0bCAS |
Trewick, S. A. (2000). Mitochondrial DNA sequences support allozyme evidence for cryptic radiation of New Zealand Peripatoides (Onychophora). Molecular Ecology 9, 269–281.
| 1:CAS:528:DC%2BD3cXisVKnu74%3D&md5=3a1b71acf90a0214d4bf114d61757d9eCAS |