Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Barcoding of mygalomorph spiders (Araneae : Mygalomorphae) in the Pilbara bioregion of Western Australia reveals a highly diverse biota

Mark A. Castalanelli A H , Roy Teale A B D , Michael G. Rix A C , W. Jason Kennington D and Mark S. Harvey A D E F G

A Department of Terrestrial Zoology, Western Australian Museum, 49 Kew Street, Welshpool, WA 6106, Australia.

B Biota Environmental Sciences Pty Ltd, PO Box 155, Leederville, WA 6903, Australia.

C Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.

D Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, WA 6009, Australia.

E Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA.

F Department of Entomology, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, USA.

G School of Natural Sciences, Edith Cowan University, Joondalup, WA 6009, Australia.

H Corresponding author. Email: mark.castalanelli@museum.wa.gov.au

Invertebrate Systematics 28(4) 375-385 http://dx.doi.org/10.1071/IS13058
Submitted: 11 November 2013  Accepted: 23 April 2014   Published: 12 September 2014

Abstract

The Pilbara bioregion of Western Australia is an area that contains vast mineral deposits and unique ecosystems. To ensure that mineral deposits are mined with minimal impact on the natural environment, impact assessment surveys are required to determine what fauna and flora species are located within proposed development areas, in particular, by determining the distributions of short-range endemic species (SREs). One infraorder of Arachnida, the Mygalomorphae (trapdoor spiders and their kin), are frequently identified as SREs. These identifications are traditionally performed using morphological techniques; however, only males can be reliably identified to species. Furthermore, the majority of species have not been formally described and males comprise only ~5% of specimens collected. To assess mygalomorph diversity and the distribution of species in the Pilbara, we employed a molecular barcoding approach. Sequence data from the mitochondrial DNA cytochrome c oxidase subunit I (COI) gene were obtained from 1134 specimens, and analysed using Bayesian methods. Only a fraction of the total mygalomorph fauna of the Pilbara has been documented, and using a species boundary cut-off of 9.5% sequence divergence, we report an increase in species richness of 191%. Barcoding provides a rapid, objective method to help quantify mygalomorph species identifications and their distributions, and these data, in turn, provide crucial information that regulatory authorities can use to assess the environmental impacts of large-scale developments.

Additional keywords: Actinopodidae, Barychelidae, Ctenizidae, Dipluridae, Idiopidae, mitochondrial DNA, Nemesiidae, speciation, Theraphosidae.


References

Armstrong, K. F., and Ball, S. L. (2005). DNA barcodes for biosecurity: invasive species identification Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1813–1823.
DNA barcodes for biosecurity: invasive species identificationCrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrjN&md5=8b4c9d1b081bf09c6a71c5e38ad3036aCAS | 16214740PubMed | open url image1

Arnedo, M. A., and Ferrández, M.-A. (2007). Mitochondrial markers reveal deep population subdivision in the European protected spider Macrothele calpeiana (Walckenaer, 1805) (Araneae, Hexathelidae). Conservation Genetics 8, 1147–1162.
Mitochondrial markers reveal deep population subdivision in the European protected spider Macrothele calpeiana (Walckenaer, 1805) (Araneae, Hexathelidae).CrossRef | 1:CAS:528:DC%2BD2sXotlSgsrY%3D&md5=874fad30b4198f031524a9b3ea36ff5fCAS | open url image1

Bond, J. E., and Stockman, A. K. (2008). An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring. Systematic Biology 57, 628–646.
An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring.CrossRef | 1:CAS:528:DC%2BD1cXhsVymsr%2FN&md5=ddbc7963a4604a6a5267264feaee6ac8CAS | 18686196PubMed | open url image1

Bond, J. E., Hendrixson, B. E., Hamilton, C. A., and Hedin, M. (2012). A reconsideration of the classification of the spider infraorder Mygalomorphae (Arachnida: Araneae) based on three nuclear genes and morphology. PLoS ONE 7, e38753.
A reconsideration of the classification of the spider infraorder Mygalomorphae (Arachnida: Araneae) based on three nuclear genes and morphology.CrossRef | 1:CAS:528:DC%2BC38XptlSntr0%3D&md5=799d079468e3d51520fd18488c543fd1CAS | 22723885PubMed | open url image1

Borges, L. M. S., Sivrikaya, H., le Roux, A., Shipway, J. R., Cragg, S. M., and Costa, F. O. (2012). Investigating the taxonomy and systematics of marine wood borers (Bivalvia: Teredinidae) combining evidence from morphology, DNA barcodes and nuclear locus sequences. Invertebrate Systematics 26, 572–582.
Investigating the taxonomy and systematics of marine wood borers (Bivalvia: Teredinidae) combining evidence from morphology, DNA barcodes and nuclear locus sequences.CrossRef | open url image1

Castalanelli, M. A., Severtson, D. L., Brumley, C. J., Szito, A., Foottit, R. G., Grimm, M., Munyard, K., and Groth, D. M. (2010). A rapid non-destructive DNA extraction method for insects and other arthropods. Journal of Asia-Pacific Entomology 13, 243–248.
A rapid non-destructive DNA extraction method for insects and other arthropods.CrossRef | 1:CAS:528:DC%2BC3cXhsFelsrvJ&md5=474c381610c7aa1bcf56f4039ba37587CAS | open url image1

Cheng, S., Lee, C. T., Wan, M. N., and Tan, S. G. (2013). Microsatellite markers uncover cryptic species of Odontotermes (Termitoidae: Termitidae) from peninsular Malaysia. Gene 518, 412–418.
Microsatellite markers uncover cryptic species of Odontotermes (Termitoidae: Termitidae) from peninsular Malaysia.CrossRef | 1:CAS:528:DC%2BC3sXit1ensrw%3D&md5=63dde52fde3e393eab70374b3eecad97CAS | 23328646PubMed | open url image1

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 | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=3cacc445e0743c5953b436bc2cf6a350CAS | 22847109PubMed | open url image1

Delsinne, T., Sonet, G., Nagy, Z. T., Wauters, N., Jacquemin, J., and Leponce, M. (2012). High species turnover of the ant genus Solenopsis (Hymenoptera: Formicidae) along an altitudinal gradient in the Ecuadorian Andes, indicated by a combined DNA sequencing and morphological approach. Invertebrate Systematics 26, 457–469.
High species turnover of the ant genus Solenopsis (Hymenoptera: Formicidae) along an altitudinal gradient in the Ecuadorian Andes, indicated by a combined DNA sequencing and morphological approach.CrossRef | 1:CAS:528:DC%2BC38XhvVKqtLrE&md5=447678dfcdc274faa281637c1035a529CAS | open url image1

Doughty, P., Rolfe, J. K., Burbridge, A. H., Pearson, D. J., and Kendrick, P. G. (2011). Herpetological assemblages of the Pilbara biogeographic region, Western Australia: ecological associations, biogeographic patterns and conservation. Records of the Western Australian Museum 78, 315–340. open url image1

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.CrossRef | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=0f644003e0450eab42e285b06371fbb5CAS | 15034147PubMed | open url image1

Environmental Protection Authority (2009). Sampling of short range endemic invertebrate fauna for environmental impact assessment in Western Australia. In ‘Guidance for the Assessment of Environmental Factors (in accordance with the Environmental Protection Act 1986). Vol. No. 20’. pp. 1–31.

Faulder, R. J. (1995). Two new species of the Australian spider genus Missulena Walckenaer (Araneae: Actinopodidae). Records of the Western Australian Museum 52, 73–78. open url image1

Finston, T. L., and Johnson, M. S. (2004). Geographic patterns of genetic diversity in subterranean amphipods of the Pilbara, Western Australia. Marine and Freshwater Research 55, 619–628.
Geographic patterns of genetic diversity in subterranean amphipods of the Pilbara, Western Australia.CrossRef | open url image1

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, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed | open url image1

Goloboff, P. A. (1993). A reanalysis of mygalomorph spider families (Araneae). American Museum Novitates 3056, 1–32. open url image1

Guthrie, N. A., Weir, T., and Will, K. (2010). Localised and regional patterns in ground-dwelling beetle assemblages in a semi-tropical arid zone environment. Records of the Western Australian Museum 78, 169–184. open url image1

Hamilton, C. A., Hendrixson, B. E., Brewer, M. S., and Bond, J. E. (2014). An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: a case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae). Molecular Phylogenetics and Evolution 71, 79–93.
An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: a case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae).CrossRef | 1:CAS:528:DC%2BC2cXhtlGktrY%3D&md5=811d748c9ccbdc3eca79ff85cf275d95CAS | 24280211PubMed | open url image1

Harms, D., and Framenau, V. W. (2013). New species of mouse spiders (Araneae: Mygalomorphae: Actinopodidae: Missulena) from the Pilbara region, Western Australia. Zootaxa 3637, 521–540. open url image1

Harvey, M. S., Berry, O., Edward, K. L., and Humphreys, G. (2008). Molecular and morphological systematics of hypogean schizomids (Schizomida: Hubbardiidae) in semiarid Australia. Invertebrate Systematics 22, 167–194.
Molecular and morphological systematics of hypogean schizomids (Schizomida: Hubbardiidae) in semiarid Australia.CrossRef | 1:CAS:528:DC%2BD1cXlslajsr8%3D&md5=3fa8e7bc708f8c1144c843f75e1b819bCAS | open url image1

Harvey, M. S., Rix, M. G., Framenau, V. W., Hamilton, Z. R., Johnson, M. S., Teale, R. J., Humphreys, G., and Humphreys, W. F. (2011). Protecting the innocent: studying short-range endemic taxa enhances conservation outcomes. Invertebrate Systematics 25, 1–10.
Protecting the innocent: studying short-range endemic taxa enhances conservation outcomes.CrossRef | open url image1

Harvey, F. S. B., Framenau, V. W., Wojcieszek, J. M., Rix, M. G., and Harvey, M. S. (2012). Molecular and morphological characterisation of new species in the trapdoor spider genus Aname (Araneae: Mygalomorphae: Nemesiidae) from the Pilbara bioregion of Western Australia. Zootaxa 3383, 15–38. open url image1

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings. Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=6937f93aeb832a9058d1fe8b082d2953CAS | open url image1

Hendrixson, B. E., and Bond, J. E. (2005). Testing species boundaries in the Antrodiaetus unicolor complex (Araneae: Mygalomorphae: Antrodiaetidae): ‘paraphyly’ and cryptic diversity. Molecular Phylogenetics and Evolution 36, 405–416.
Testing species boundaries in the Antrodiaetus unicolor complex (Araneae: Mygalomorphae: Antrodiaetidae): ‘paraphyly’ and cryptic diversity.CrossRef | 15955518PubMed | open url image1

Hickman, A. H. (2012). Review of the Pilbara Craton and Fortescue Basin, Western Australia: Crustal evolution providing environments for early life. The Island Arc 21, 1–31.
Review of the Pilbara Craton and Fortescue Basin, Western Australia: Crustal evolution providing environments for early life.CrossRef | open url image1

Hogg, H. R. (1903). Two new Australian spiders of the family Ctenizidae. Annals & Magazine of Natural History 11, 308–312.
Two new Australian spiders of the family Ctenizidae.CrossRef | open url image1

Humphreys, W. F. (2001). Groundwater calcrete aquifers in the Australian arid zone: the context to an unfolding plethora of stygal biodiversity. Records of the Western Australian Museum 64, 63–83. open url image1

Main, B. Y. (1983). Further studies on the systematics of Australian Diplurinae (Chelicerata: Mygalomorphae: Dipluridae): two new genera from south western Australia. Journal of Natural History 17, 923–949.
Further studies on the systematics of Australian Diplurinae (Chelicerata: Mygalomorphae: Dipluridae): two new genera from south western Australia.CrossRef | open url image1

Main, B. Y. (1985a). Further studies on Australian Diplurinae: a review of the genera of the Teylini (Araneae: Mygalomorphae: Dipluridae). Australian Journal of Zoology 33, 743–759.
Further studies on Australian Diplurinae: a review of the genera of the Teylini (Araneae: Mygalomorphae: Dipluridae).CrossRef | open url image1

Main, B. Y. (1985b). Further studies on the systematics of ctenizid trapdoor spiders: a review of the Australian genera (Araneae: Mygalomorphae: Ctenizidae). Australian Journal of Zoology. Supplementary Series 33, 1–84.
Further studies on the systematics of ctenizid trapdoor spiders: a review of the Australian genera (Araneae: Mygalomorphae: Ctenizidae).CrossRef | open url image1

Main, B. Y. (2004). Biosystematics of Australian mygalomorph spiders: descriptions of three new species of Teyl from Victoria (Araneae: Nemesiidae). Memoirs of Museum Victoria 61, 47–55. open url image1

Martínez, J. J., Berta, C., Varone, L., Logarzo, G., Zamudio, P., Zaldívar-Riverón, A., and Aguilar-Velasco, R. G. (2012). DNA barcoding and morphological identification of Argentine species of Apanteles (Hymenoptera: Braconidae), parasitoids of cactus-feeding moths (Lepidoptera: Pyralidae: Phycitinae), with description of a new species. Invertebrate Systematics 26, 435–444.
DNA barcoding and morphological identification of Argentine species of Apanteles (Hymenoptera: Braconidae), parasitoids of cactus-feeding moths (Lepidoptera: Pyralidae: Phycitinae), with description of a new species.CrossRef | open url image1

Meiklejohn, K. A., Wallman, J. F., Cameron, S. L., and Dowton, M. (2012). Comprehensive evaluation of DNA barcoding for the molecular species identification of forensically important Australian Sarcophagidae (Diptera). Invertebrate Systematics 26, 515–525.
Comprehensive evaluation of DNA barcoding for the molecular species identification of forensically important Australian Sarcophagidae (Diptera).CrossRef | 1:CAS:528:DC%2BC38XhvVKqtLvI&md5=874558744bd89e8dbe15b0d321e75dd3CAS | open url image1

Pedersen, A. A., and Loeschcke, V. (2001). Conservation genetics of peripheral populations of the mygalomorph spider Atypus affinis (Atypidae) in northern Europe. Molecular Ecology 10, 1133–1142.
Conservation genetics of peripheral populations of the mygalomorph spider Atypus affinis (Atypidae) in northern Europe.CrossRef | 1:CAS:528:DC%2BD3MXktFKitbo%3D&md5=e25ac61013ffa78b196127108c9b7014CAS | 11380872PubMed | open url image1

Pepper, M., Fujita, M. K., Moritz, C., and Keogh, J. S. (2011). Palaeoclimate change drove diversification among isolated mountain refugia in the Australian arid zone. Molecular Ecology 20, 1529–1545.
Palaeoclimate change drove diversification among isolated mountain refugia in the Australian arid zone.CrossRef | 21371147PubMed | open url image1

Pepper, M., Doughty, P., and Keogh, J. S. (2013). Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium. Journal of Biogeography 40, 1225–1239.
Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium.CrossRef | open url image1

Pocock, R. I. (1897). On some trapdoor spiders of the family Ctenizidae from South and West Australia, contained in the collection of the British Museum. The Annals and Magazine of Natural History 6(19), 109–116.

Raven, R. J. (1985). The spider infraorder Mygalomorphae (Araneae): cladistics and systematics. Bulletin of the American Museum of Natural History 182, 1–180. open url image1

Raven, R. J. (1994). Mygalomorph spiders of the Barychelidae in Australia and the western Pacific. Memoirs of the Queensland Museum 35, 291–706. open url image1

Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MRBAYES 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=d5b84f5cc16cfb75b367ced57a76cb2cCAS | 12912839PubMed | open url image1

Thackway, R., and Cresswell, I. D. (1995). An interim biogeographic regionalisation for Australia: a framework for setting priorities in the National Reserves System Cooperative Program, Version 4.0. (ANC Agency: Canberra.)

Volschenk, E. S., Burbidge, A. H., Durrant, B. J., and Harvey, M. S. (2010). Spatial patterns of scorpions (Scorpiones) in the arid Pilbara region of Western Australia. Records of the Western Australian Museum 78, 271–284. open url image1

Wishart, G., and Rowell, D. M. (2008). Trapdoor spiders of the genus Misgolas (Mygalomorphae: Idiopidae) from eastern New South Wales, with notes on genetic variation. Records of the Australian Museum 60, 45–86.
Trapdoor spiders of the genus Misgolas (Mygalomorphae: Idiopidae) from eastern New South Wales, with notes on genetic variation.CrossRef | open url image1

Zhou, Z. J., Li, R. L., Huang, D. W., and Shi, F. M. (2012). Molecular identification supports most traditional morphological species of Ruspolia (Orthoptera: Conocephalinae). Invertebrate Systematics 26, 451–456.
Molecular identification supports most traditional morphological species of Ruspolia (Orthoptera: Conocephalinae).CrossRef | open url image1



Supplementary MaterialSupplementary Material 144.4 KB Export Citation