Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE (Open Access)

Integrative taxonomy of the stick insect genus Austrocarausius Brock, 2000 (Phasmatodea: Lonchodidae) reveals cryptic species in remnant Queensland rainforests

Braxton R. Jones https://orcid.org/0000-0002-1545-8415 A * , Paul D. Brock B , Barbara Mantovani C , Perry Beasley-Hall A D E , David K. Yeates F and Nathan Lo A
+ Author Affiliations
- Author Affiliations

A School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia.

B The Natural History Museum, Cromwell Road, London, SW7 5BD, UK.

C Department of Biological, Geological and Environmental Sciences, University of Bologna, I-40126 Bologna, Italy.

D School of Biological Sciences, The University of Adelaide, Adelaide, SA 5000, Australia.

E South Australian Museum, Adelaide, SA 5000, Australia.

F Australian National Insect Collection, CSIRO PO Box 1700, Canberra, ACT 2601, Australia.

* Correspondence to: braxton926@gmail.com

Handling Editor: Andy Austin

Invertebrate Systematics 36(9) 849-873 https://doi.org/10.1071/IS21076
Submitted: 12 November 2021  Accepted: 28 July 2022   Published: 21 September 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Austrocarausius Brock, 2000 is a stick insect (Phasmatodea: Lonchodidae) genus containing two species restricted to the tropical rainforests of northern Queensland. Recent specimen collections between the two species’ type localities, Lizard Island and Rockhampton, have suggested that Austrocarausius might represent more than the two nominal species. Here, we apply morphological and molecular analyses to revise the taxonomy of this genus. Using both field-collected and historic museum samples, we developed morphological species hypotheses and descriptions. Genetic sequencing of mitochondrial COI and 16S were undertaken for species delimitation and phylogenetic analysis, including an estimate of the evolutionary timescale of the genus. Based on these results, we propose nine new Austrocarausius species, increasing the number of species in the genus to eleven: A. nigropunctatus (Kirby, 1896), A. mercurius (Stål, 1877), A. coronatus sp. nov., A. decorus sp. nov., A. eirmosus sp. nov., A. gasterbulla sp. nov., A. tuberosus sp. nov., A. macropunctatus sp. nov., A. truncatus sp. nov. A. waiben sp. nov. and A. walkeri sp. nov. Our results suggest Austrocarausius species diversified over the last c. 25–70 Ma, resulting in the now endemic distributions in the tropical rainforests of the central and northern Queensland coasts. This is the first integrative systematic study of an Australian phasmid genus, combining morphological, molecular and biogeographical methods. Additional species of Austrocarausius likely remain undescribed as can be inferred from methodical sampling of rainforest patches along the Queensland coast.

Keywords: biogeography, dispersal, integrative taxonomy, molecular dating, morphological analysis, phylogenetic, systematics, taxonomy.


References

Balderson J, Rentz DCF, Roach AME (1998) Phasmatodea. In ‘Zoological Catalogue of Australia. Vol. 23. Archaeognatha, Zygentoma, Blattodea, Isoptera, Mantodea, Dermaptera, Phasmatodea, Embioptera, Zoraptera’. (Eds WWK Houston, A Wells) pp. 347–376, 451–456. (CSIRO Publishing: Melbourne, Vic., Australia)

Bouckaert, RR, and Drummond, AJ (2017). bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17, 42.
bModelTest: Bayesian phylogenetic site model averaging and model comparison.Crossref | GoogleScholarGoogle Scholar |

Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, CH, Xie, D, Suchard, MA, Rambaut, A, and Drummond, AJ (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar |

Bragg PE (2001) ‘Phasmids of Borneo.’ (Natural History Publications: Kota Kinabalu, Malaysia)

Brock, PD (2000). Studies on Australian stick-insects of the Family Heteronemiidae, Subfamily Lonchodinae, including the description of a new genus. Journal of Orthoptera Research 9, 51–55.
Studies on Australian stick-insects of the Family Heteronemiidae, Subfamily Lonchodinae, including the description of a new genus.Crossref | GoogleScholarGoogle Scholar |

Brock, PD, and Hasenpusch, J (2007). Studies on the Australian stick insects (Phasmida), including a checklist of species and bibliography. Zootaxa 1570, 1–84.
Studies on the Australian stick insects (Phasmida), including a checklist of species and bibliography.Crossref | GoogleScholarGoogle Scholar |

Brock PD, Hasenpusch JW (2009) ‘The complete field guide to stick and leaf insects of Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Brock, PD, and Monteith, GB (2018). A striking new species of Parapodacanthus Brock (Phasmida: Phasmatidae) from southeastern Queensland. Australian Entomologist 45, 17–26.

Brunner von Wattenwyl K (1907) ‘Die Insektenfamilie der Phasmiden. Vol. 2. Phasmidae Anareolatae (Clitumnini, Lonchodini, Bacunculini)’. pp. 181–340. (Wilhelm Engelmann: Leipzig: German Empire)

Byrne, M, Yeates, DK, Joseph, L, Kearney, M, Bowler, J, Williams, MAJ, Cooper, S, Donnellan, SC, Keogh, JS, Leys, R, Melville, J, Murphy, DJ, 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 |

Byrne, M, Steane, DA, Joseph, L, Yeates, DK, Jordan, GJ, Crayn, D, Aplin, K, Cantrill, DJ, Cook, LG, Crisp, MD, Keogh, JS, Melville, J, Moritz, C, Porch, N, Sniderman, JMK, Sunnucks, P, and Weston, PH (2011). Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. Journal of biogeography 38, 1635–1656.
Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota.Crossref | GoogleScholarGoogle Scholar |

Cliquennois N (2020) Chapter 18 Ordre des Phasmatodea (Phasmes). In ‘Les Insectes du Monde Biodiversité, classification, clés de détermination des familles’. (Ed. H-P Aberlenc) Vol. 1, pp. 403–437. (Éditions Quae: France)

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

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

Edgar, RC (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 | 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, 294–299.

Fourment, M, and Holmes, EC (2016). Seqotron: a user-friendly sequence editor for Mac OS X. BMC Research Notes 9, 106.
Seqotron: a user-friendly sequence editor for Mac OS X.Crossref | GoogleScholarGoogle Scholar |

Greenwood DR, Christophel DC (2005) The origins and tertiary history of Australian ‘tropical’ rainforests. In ‘Tropical rainforests: past, present and future’. pp. 336–373. (University of Chicago Press: Chicago, IL, USA)

Hennemann, FH, and Conle, OV (2008). Revision of Oriental Phasmatodea: the tribe PharnaciiniGünther, 1953, including the description of the world's longest insect, and a survey of the family Phasmatidae Gray, 1835 with keys to the subfamilies and tribes (Phasmatodea: Anareolatae: Phasmatidae). Zootaxa 1906, 1–316.

Kapli, P, Lutteropp, S, Zhang, J, Kobert, K, Pavlidis, P, Stamatakis, A, and Flouri, T (2017). Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638.
Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo.Crossref | GoogleScholarGoogle Scholar |

Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, and Drummond, A (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |

Kirby, WF (1896). VI. On some new or rare Phasmidae in the collection of the British Museum. Transactions of the Linnean Society of London. 2nd Series. Zoology 6, 447–475.
VI. On some new or rare Phasmidae in the collection of the British Museum.Crossref | GoogleScholarGoogle Scholar |

Kirby WF (1904) ‘A synonymic catalogue of Orthoptera. I. Orthoptera Euplexoptera, Cursoria et Gressoria).’ (British Museum Natural History: London, UK)
| Crossref |

Moreau, CS, Hugall, AF, McDonald, KR, Jamieson, BGM, and Moritz, C (2015). An ancient divide in a contiguous rainforest: endemic earthworms in the Australian Wet Tropics. PLoS One 10, e0136943.
An ancient divide in a contiguous rainforest: endemic earthworms in the Australian Wet Tropics.Crossref | GoogleScholarGoogle Scholar |

Otte D, Brock P (2005) ‘Phasmida Species File. Catalog of the Stick and Leaf Insects of the World’, 2nd edn. (Insect Diversity Association: Philadelphia, PA, USA)

Poinar, G Jr (2011). A walking stick, Clonistria dominicana n. sp. (Phasmatodea: Diapheromeridae) in Dominican amber. Historical Biology 23, 223–226.
A walking stick, Clonistria dominicana n. sp. (Phasmatodea: Diapheromeridae) in Dominican amber.Crossref | GoogleScholarGoogle Scholar |

Puillandre, N, Lambert, A, Brouillet, S, and Achaz, G (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar |

Rainbow, WJ (1897). Description of two new Australian Phasmas, together with a synopsis of the Phasmidae in Australia. Records of the Australian Museum 3, 34–37.
Description of two new Australian Phasmas, together with a synopsis of the Phasmidae in Australia.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A, Drummond, AJ, Xie, D, Baele, G, and Suchard, MA (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar |

Rix, MG, and Harvey, MS (2012). Phylogeny and historical biogeography of ancient assassin spiders (Araneae: Archaeidae) in the Australian mesic zone: evidence for Miocene speciation within Tertiary refugia. Molecular Phylogenetics and Evolution 62, 375–396.
Phylogeny and historical biogeography of ancient assassin spiders (Araneae: Archaeidae) in the Australian mesic zone: evidence for Miocene speciation within Tertiary refugia.Crossref | GoogleScholarGoogle Scholar |

Robertson, JA, Bradler, S, and Whiting, MF (2018). Evolution of oviposition techniques in stick and leaf insects (Phasmatodea). Frontiers in Ecology and Evolution 6, 216.
Evolution of oviposition techniques in stick and leaf insects (Phasmatodea).Crossref | GoogleScholarGoogle Scholar |

Rudolf E, Brock P (2017) Plain stick-insect Austrocarausius mercurius. In ‘The IUCN Red List of Threatened Species 2017’. e.T78789295A78792052. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/78789295/78792052 [Verified 29 July 2022]

Sellick, JTC (1994). Phasmida (stick insect) eggs from the Eocene of Oregon. Palaeontology 37, 913–922.

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.
Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar |

Simon, S, Letsch, H, Bank, S, Buckley, TR, Donath, A, Liu, S, Machida, R, Meusemann, K, Misof, B, Podsiadlowski, L, Zhou, X, Wipfler, B, and Bradler, S (2019). Old World and New World Phasmatodea: phylogenomics resolve the evolutionary history of stick and leaf insects. Frontiers in Ecology and Evolution 7, 345.
Old World and New World Phasmatodea: phylogenomics resolve the evolutionary history of stick and leaf insects.Crossref | GoogleScholarGoogle Scholar |

Stål, C (1877). Espèces nouvelles de Phasmides. Annales de la Société Entomologique de Belgique, Comptes Rendues 20, 62–68.

Tepper, JGO (1903). List of described genera and species of the Australian and Polynesian Phasmidae (Spectre-insects). Transactions of the Royal Society of Southern Australia 26, 278–287.

Trifinopoulos, J, Nguyen, LT, von Haeseler, A, and Minh, BQ (2016). W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, W232–W235.
W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis.Crossref | GoogleScholarGoogle Scholar |

Velonà, A, Brock, PD, Hasenpusch, J, and Mantovani, B (2015). Cryptic diversity in Australian stick insects (Insecta; Phasmida) uncovered by the DNA barcoding approach. Zootaxa. 3957, 455–466.
Cryptic diversity in Australian stick insects (Insecta; Phasmida) uncovered by the DNA barcoding approach.Crossref | GoogleScholarGoogle Scholar |

Vickery VR (1983) Catalogue of Australian stick insects (Phasmida, Phasmatodea, Phasmatoptera, or Cheleutoptera). CSIRO Division of Entomology, Technical Paper 20, CSIRO, Melbourne, Vic., Australia.

Will, KW, Mishler, BD, and Wheeler, QD (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54, 844–851.
The perils of DNA barcoding and the need for integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |

Wedmann, S, Bradler, S, and Rust, J (2007). The first fossil leaf insect: 47 million years of specialized cryptic morphology and behavior. Proceedings of the National Academy of Sciences 104, 565–569.

Yeates, DK, Seago, A, Nelson, L, Cameron, SL, Joseph, L, and Trueman, JWH (2010). Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36, 209–217.
Integrative taxonomy, or iterative taxonomy?Crossref | GoogleScholarGoogle Scholar |