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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular phylogenetic analysis of Western Australian troglobitic chthoniid pseudoscorpions (Pseudoscorpiones : Chthoniidae) points to multiple independent subterranean clades

Sophie E. Harrison A C , Michelle T. Guzik A , Mark S. Harvey B and Andrew D. Austin A
+ Author Affiliations
- Author Affiliations

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

B Department of Terrestrial Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, WA 6986, Australia; School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia; School of Natural Sciences, Edith Cowan University, Joondalup, WA 6027, Australia; Research Associate, Division of Invertebrate Zoology, American Museum of Natural History, New York, USA; Research Associate, Department of Entomology, California Academy of Sciences, San Francisco, CA, USA.

C Corresponding author. Email: sophie.e.harrison@adelaide.edu.au

Invertebrate Systematics 28(4) 386-400 https://doi.org/10.1071/IS14005
Submitted: 13 January 2014  Accepted: 16 May 2014   Published: 12 September 2014

Abstract

The Yilgarn and Pilbara regions of Western Australia are considered biodiversity hotspots for subterranean invertebrates. While the relatively well studied (aquatic) stygofauna are typically constrained to geographically isolated habitats (‘subterranean islands’) and have likely originated from multiple independent epigean ancestors, the troglofauna found in cavernicolous calcretes and fractured rock remains largely unstudied. Here we focus on the pseudoscorpion genera Tyrannochthonius Chamberlin, 1929 and Lagynochthonius Beier, 1951, as common components of the troglofauna, to determine whether they also display highly restricted distributional patterns, and have independent origins. Bayesian and maximum likelihood analyses of sequence data from the mtDNA cytochrome c oxidase I (COI) and the small subunit 18S nuclear genes for subterranean and epigean species from both genera reveal divergent mtDNA lineages that are restricted to single aquifers and/or geographic locations. This strong geographic structuring of troglobitic pseudoscorpions is indicative of short-range endemism and supports the ‘subterranean island’ hypothesis. Further, independent sister relationships between subterranean and epigean taxa indicate multiple invasions into subterranean habitats, likely driven by post-Miocene aridification, consistent with that predicted for the stygofauna. The phylogeny also reveals that Tyrannochthonius + Lagynochthonius is monophyletic but that Lagynochthonius is polyphyletic and nested inside Tyrannochthonius. The results of this study point to common processes that have shaped the diversity and uniqueness of both stygofaunal and troglofaunal communities in Western Australia.

Additional keywords: 18S, aquifer, cytochrome c oxidase 1, Pilbara, short-range endemic, troglofauna, Yilgarn.


References

Arabi, J., Judson, M. L., Deharveng, L., Lourenço, W. R., Cruaud, C., and Hassanin, A. (2012). Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenic rearrangements. Journal of Molecular Evolution 74, 81–95.
Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenic rearrangements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xktlaktr0%3D&md5=e79441b6d22a87576be6bdf0b30b8360CAS | 22362465PubMed |

Beier, M. (1951). Die Pseudoscorpioniden Neu-Guineas und der benachbarten Inseln. Pacific Insects 7, 749–796.

Beier, M. (1965). Die Pseudoscorpion Indochinas. Memoires du Museum National d’Histoire Naurelle, Paris, Nouvelle Serie 1, 47–123.

Beier, M. (1973). Pseudoscorpionidea von Ceylon. Entomologica Scandinavica 4, 39–55.

Byrne, M., Yeates, D. K., Joseph, L., Kearney, M., Bowler, J., Williams, M. A., Cooper, S., Donnellan, S. C., Keogh, J. S., Leys, R., Melville, J., Murphy, D. J., Porch, N., and Wyrwoll, K. H. (2008). Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=48c6ce0fa50c826d8ecb937c38093413CAS | 18761619PubMed |

Chamberlin, J. C. (1962). New and little-known false scorpions, principally from caves, belonging to the families Chthoniidae and Neobisiidae. Bulletin of the American Museum of Natural History 123, 303–352.

Cooper, S., Hinze, S., Leys, R., Watts, C. H. S., and Humphreys, W. F. (2002). Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia. Invertebrate Systematics 16, 589–598.
Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia.Crossref | GoogleScholarGoogle Scholar |

Cooper, S., Bradbury, J. H., Saint, K. M., Remko, L., Austin, A. D., and Humphreys, W. F. (2007). Subterranean achipelago in the Australian arid zone: mitochondiral DNA phylogeography of amphipods from central Western Australia. Molecular Ecology 16, 1533–1544.
Subterranean achipelago in the Australian arid zone: mitochondiral DNA phylogeography of amphipods from central Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Gmu7w%3D&md5=5e73081a9e82631a42e2ff61df9c077cCAS | 17391274PubMed |

Cooper, S., Saint, K. M., Taiti, S., Austin, A. D., and Humphreys, W. F. (2008). Subterranean archipelago: mitochondrial DNA phylogeography of stygobitic isopods (Oniscidea: Haloniscus) from the Yilgarn region of Western Australia. Invertebrate Systematics 22, 195–203.
Subterranean archipelago: mitochondrial DNA phylogeography of stygobitic isopods (Oniscidea: Haloniscus) from the Yilgarn region of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Crayn, D. M., Rossetto, M., and Maynard, D. J. (2006). Molecular phylogeny and dating reveals an Oligo-Miocene radiation of dry-adapted shrubs (former Tremandraceae) from rainforest tree progenitors (Elaeocarpaceae) in Australia. American Journal of Botany 93, 1328–1342.
Molecular phylogeny and dating reveals an Oligo-Miocene radiation of dry-adapted shrubs (former Tremandraceae) from rainforest tree progenitors (Elaeocarpaceae) in Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFGrtb3J&md5=2130cf6c3346c7da86d856ad47e93bc0CAS | 21642198PubMed |

Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2011). Geneious v5.4. Available from http://www.geneious.com/ [Verified July 2014]

Eberhard, S. M., Halse, S. A., and Humphreys, W. F. (2005). Stygofauna in the Pilbara region, north-west Western Australia: a review. Journal of the Royal Society of Western Australia 88, 167–176.

Edgecombe, G. D. (2005). A troglomorphic species of the centipede Cryptops (Trigonocryptops) (Chilopoda: Scolopendromorpha) from Western Australia. Records of the Western Australian Museum 22, 315–323.

Edward, K. L., and Harvey, M. S. (2008). Short-range endemism in hypogean environments: the pseudoscorpion genera Tyrannochthonius and Lagynochthonius (Pseudoscorpiones: Chthoniidae) in the semiaird zone of Western Australia. Invertebrate Systematics 22, 259–293.
Short-range endemism in hypogean environments: the pseudoscorpion genera Tyrannochthonius and Lagynochthonius (Pseudoscorpiones: Chthoniidae) in the semiaird zone of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Erixon, P., Svennblad, B., Britton, T., and Oxelman, B. (2003). Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Systematic Biology 52, 665–673.
Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics.Crossref | GoogleScholarGoogle Scholar | 14530133PubMed |

Finston, T. L., Bradbury, J. H., and Johnson, M. S. (2004). When morphology and molecular markers conflict: a case history of subterranean amphipods from the Pilbara, Western Australia. Animal Biodiversity and Conservation 27, 83–94.

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 |

Guzik, M. T., Abrams, K. M., Cooper, S. B., Humphreys, W. F., Cho, J. L., and Austin, A. D. (2008). Phylogeography of the ancient Parabathynellidae (Crustacea: Bathynellacea) from the Yilgarn region of Western Australia. Invertebrate Systematics 22, 205–216.
Phylogeography of the ancient Parabathynellidae (Crustacea: Bathynellacea) from the Yilgarn region of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Guzik, M. T., Austin, A. D., Cooper, S. J. B., Harvey, M. S., Humphreys, W. F., Bradford, T., Eberhard, S. M., King, R. A., Leijs, R., Muirhead, K. A., and Tomlinson, M. (2011). Is the Australian subterranean fauna uniquely diverse? Invertebrate Systematics 24, 407–418.
Is the Australian subterranean fauna uniquely diverse?Crossref | GoogleScholarGoogle Scholar |

Harvey, M. S. (2002). Short-range endemism amongst the Australian fauna: some examples from non-marine environments. Invertebrate Systematics 16, 555–570.
Short-range endemism amongst the Australian fauna: some examples from non-marine environments.Crossref | GoogleScholarGoogle Scholar |

Harvey, M. S. (2013). Pseudoscorpions of the world, version 3.0. Western Australian Museum, Perth. Available at http://museum.wa.gov.au/catalogues-beta/pseudoscorpions (Accessed 4 April 2014.)

Harvey, M. S., and Edward, K. L. (2007). A review of the pseudoscorpion genus Ideoblothrus (Pseudoscorpiones, Syarinidae) from western and northern Australia. Journal of Natural History 41, 445–472.
A review of the pseudoscorpion genus Ideoblothrus (Pseudoscorpiones, Syarinidae) from western and northern Australia.Crossref | GoogleScholarGoogle Scholar |

Harvey, M. S., and Volschenk, E. S. (2007). The systematics of the Gondwanan pseudoscorpion family Hyidae (Pseudoscorpiones: Neobisioidea): new data and a revised phylogenetic hypothesis. Invertebrate Systematics 21, 365–406.
The systematics of the Gondwanan pseudoscorpion family Hyidae (Pseudoscorpiones: Neobisioidea): new data and a revised phylogenetic hypothesis.Crossref | GoogleScholarGoogle Scholar |

Harvey, M. S., Shear, W. A., and Hoch, H. (2000). Onychophora, Arachnida, myriapods and Insecta. In ‘Subterranean Ecosystems’. (Eds H. Wilkens, D.C. Culver and W.F. Humphreys.) pp. 79–94. (Elsevier: Amsterdam.)

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslajsr8%3D&md5=3fa8e7bc708f8c1144c843f75e1b819bCAS |

Howarth, F. G. (1988). Environmental ecology of north Queensland caves: or why are there so many troglobites in Australia? In ‘Speleological Federation Tropicon Conference, Lake Tinaroo, Far North Queensland’. (Ed. L. Pearson.) pp. 76–84. (Australian Speleological Federation: Cairns, Australia.)

Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
MRBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=ceab3d44bc74e85c441d4509c0328141CAS | 11524383PubMed |

Hugall, A., Moritz, C., Moussalli, A., and Stanisic, J. (2002). Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proceedings of the National Academy of Sciences of the United States of America 99, 6112–6117.
Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslWnsrk%3D&md5=d71534746b8dc0b9a6a0402d5ccab4faCAS | 11972064PubMed |

Humphreys, W. F. (1990). The biology of a troglobitic schizomid (Chelicerata: Arachnida) from caves in the semi-arid Cape Range, Western Australia. Acta Zoologica Fennica 190, 181–186.

Humphreys, W. F., and Shear, W. A. (1993). Troglobitic millipedes (Diplopoda: Paradoxosomatidae) from semi-arid Cape Range, Western Australia: systematics and biology. Invertebrate Taxonomy 7, 173–195.
Troglobitic millipedes (Diplopoda: Paradoxosomatidae) from semi-arid Cape Range, Western Australia: systematics and biology.Crossref | GoogleScholarGoogle Scholar |

Judson, M. L. I. (2007). A new and endangered species of the pseudoscorpion genus Lagynochthonius from a cave in Vietnam, with notes on chelal morphology and the composition of the Tyrannochthoniini (Arachnida, Chelonethi, Chthoniidae). Zootaxa 1627, 53–68.

Krajewski, C., Wroe, S., and Westerman, M. (2000). Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zoological Journal of the Linnean Society 130, 375–404.
Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials.Crossref | GoogleScholarGoogle Scholar |

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=6252e96674fb862520ea0b491079d71fCAS | 22319168PubMed |

Leys, R., and Watts, C. H. (2008). Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus. Invertebrate Systematics 22, 217–225.
Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus.Crossref | GoogleScholarGoogle Scholar |

Leys, R., Watts, C. S., Cooper, S. B., and Humphreys, W. F. (2003). Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834.
| 14761060PubMed |

Mahnert, V. (1986). Die Pseudoskorpione (Arachnida) Kenyas. VIII. Chthoniidae. Revue Suisse de Zoologie 92, 823–843.

Mahnert, V. (1988). Une nouvelle espèce du genre Tyrannochthonius (Lagynochthonius) (Pseudoscorpiones: Chthoniidae) des grottes de Sarawak (Malaysia). Archives des Sciences, Genève 41, 383–386.

Muchmore, W. B. (1984). Pseudoscorpions from Florida and the Caribbean area. 13. New species of Tyrannochthonius and Paraliochthonius from the Bahamas, with discussion of the genera (Chthoniidae). The Florida Entomologist 67, 119–126.
Pseudoscorpions from Florida and the Caribbean area. 13. New species of Tyrannochthonius and Paraliochthonius from the Bahamas, with discussion of the genera (Chthoniidae).Crossref | GoogleScholarGoogle Scholar |

Muchmore, W. B. (1991). Pseudoscorpions from Florida and the Caribbean area. 14. New species of Tyrannochthonius and Lagynochthonius from caves in Jamacia [sic], with discussion of the genera (Chthoniidae). The Florida Entomologist 74, 110–121.
Pseudoscorpions from Florida and the Caribbean area. 14. New species of Tyrannochthonius and Lagynochthonius from caves in Jamacia [sic], with discussion of the genera (Chthoniidae).Crossref | GoogleScholarGoogle Scholar |

Muchmore, W. B. (2000). The Pseudoscorpionida of Hawaii Part I. Introduction and Chthonioidea. Proceedings of the Entomological Society of Hawaii 34, 147–162.

Murienne, J., Harvey, M. S., and Giribet, G. (2008). First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata). Molecular Phylogenetics and Evolution 49, 170–184.
First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltrzP&md5=05dd5f34c002757f0ac106b25a803982CAS | 18603009PubMed |

Murphy, D. J., Miller, J. T., Bayer, R. J., and Ladiges, P. Y. (2003). Molecular phylogeny of Acacia subgenus Phyllodineae (Mimosoideae: Leguminosae) based on DNA sequences of the internal transcribed spacer region. Australian Systematic Botany 16, 19–26.
Molecular phylogeny of Acacia subgenus Phyllodineae (Mimosoideae: Leguminosae) based on DNA sequences of the internal transcribed spacer region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1yru78%3D&md5=18d1f25e697d7a1fa745257e67285931CAS |

Rambaut, A., and Drummond, A. J. (2007). Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer.

Schmidt, H. A., Strimmer, K., Vingron, M., and von Haeseler, A. (2002). TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504.
| 1:CAS:528:DC%2BD38XivFKrsL0%3D&md5=ab1e38a462590d87e9973931d2dd59ffCAS | 11934758PubMed |

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=d5c73c20640b01d4cb1718c8d993d994CAS |

Simon, C., Buckley, T. R., Francesco, F., Stewart, J. B., and Beckenbach, A. T. (2006). Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics 37, 545–579.
Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |

Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. In ‘Bioinformatics’, open access.

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=5ee5a71f721d24a7782516dc0ff5fcfcCAS | 21546353PubMed |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=7195ccc0c11241cf9fe1f6a3cd609934CAS | 24132122PubMed |

Truswell, E. M. (1990). Australian rainforests: the 100 million year record. In ‘Australian Tropical Rainforests’. (Eds L.J. Webb and J. Kikkawa.) pp. 1–22. (CSIRO: East Melbourne.)

Volschenk, E. S., and Prendini, L. (2008). Aops oncodactylus, gen. et sp. nov., the first troglobitic urodacid (Urodacidae: Scorpiones), with a re-assessment of cavernicolous, troglobitic and troglomorphic scorpions. Invertebrate Systematics 22, 235–257.
Aops oncodactylus, gen. et sp. nov., the first troglobitic urodacid (Urodacidae: Scorpiones), with a re-assessment of cavernicolous, troglobitic and troglomorphic scorpions.Crossref | GoogleScholarGoogle Scholar |

Weygoldt, P. (1969). ‘The Biology of Pseudoscorpions.’ (Harvard University Press: Cambridge, MA.)

Whiting, M. F. (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.
Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera.Crossref | GoogleScholarGoogle Scholar |