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

Phylogenomics of endemic Australian Ulopinae (Hemiptera: Cicadomorpha: Cicadellidae)

Olivia Evangelista https://orcid.org/0000-0001-8515-3548 A * , Nikolai Tatarnic B C and Keith Bayless A D
+ Author Affiliations
- Author Affiliations

A Australian National Insect Collection, CSIRO, Canberra, ACT 2601, Australia.

B Collections and Research Centre, Western Australian Museum, Locked Bag 49, Welshpool DC, Perth, WA 6106, Australia.

C Centre for Evolutionary Biology, University of Western Australia, Crawley, WA 6009, Australia.

D Australian Museum, Sydney, NSW 2010, Australia.

* Correspondence to: olivia.evangelista@csiro.au

Handling Editor: Prashant Sharma

Invertebrate Systematics 38, IS23035 https://doi.org/10.1071/IS23035
Submitted: 10 July 2023  Accepted: 15 January 2024  Published: 13 February 2024

© 2024 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

Ulopinae is a distinctive subfamily of leafhoppers that is widely distributed across the Afrotropical, Palearctic, Indomalayan and Australasian regions. The ulopine fauna of Australia is entirely endemic and includes two tribes of striking appearance, the Ulopini and Cephalelini. Knowledge of these groups is fragmentary and in many instances, no information is available beyond original descriptions. We assess the monophyly, phylogenetic placement and species-level diversity of the Ulopini genus Austrolopa. Phylogenetic analyses based on sequence data from target nuclear loci (18S, 28S, H2A and H3) and mitochondrial genomes (15 genes) for 23 membracoid taxa yielded congruent topologies. Our results provide strong evidence for the monophyly of Ulopinae and a clade consisting of Ulopini + Cephalelini. However, a non-monophyletic Cephalelini arises from within a polyphyletic Ulopini. Austrolopa was strongly recovered as monophyletic in all analyses, a result also supported by morphological features. The genus currently includes six species, three of which are described based on morphological and molecular data: Austrolopa botanica, sp. nov., Austrolopa rotunda, sp. nov. and Austrolopa sublima, sp. nov. A lectotype designation is provided for Austrolopa kingensis Evans, 1937, sp. reval. Our findings illustrate that the Australian Ulopinae is far more diverse than currently circumscribed and several species of Austrolopa are yet to be recognised.

ZooBank: urn:lsid:zoobank.org:pub:1480285B-8F61-4659-A929-2B1EF3168868

Keywords: Austrolopa, Bush Blitz, bush fires, leafhoppers, Membracoide, narrow-range endemics, species discovery, Ulopini.

References

Allio R, Schomaker-Bastos A, Romiguier J, Prosdocimi F, Nabholz B, Delsuc F (2020) MitoFinder: efficient automated large-scale extraction of mitogenomic data in target enrichment phylogenomics. Molecular Ecology Resources 20(4), 892-905.
| Crossref | Google Scholar | PubMed |

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19(5), 455-477.
| Crossref | Google Scholar | PubMed |

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-20.
| Crossref | Google Scholar | PubMed |

Borowiec ML (2016) AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4, e1660.
| Crossref | Google Scholar | PubMed |

Bushnell B, Rood J, Singer E (2017) BBMerge – accurate paired shotgun read merging via overlap. PLoS One 12(10), e0185056.
| Crossref | Google Scholar | PubMed |

Cai L, Zhang H, Davis CC (2022) PhyloHerb: a high-throughput phylogenomic pipeline for processing genome skimming data. Applications in Plant Sciences 10(3), e11475.
| Crossref | Google Scholar | PubMed |

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10, 421.
| Crossref | Google Scholar | PubMed |

Cao Y, Dietrich CH, Zahniser JN, Dmitriev DA (2022) Dense sampling of taxa and characters improves phylogenetic resolution among deltocephaline leafhoppers (Hemiptera: Cicadellidae: Deltocephalinae). Systematic Entomology 47(3), 430-444.
| Crossref | Google Scholar |

Cryan JR, Urban JM (2012) Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic? Systematic Entomology 37(1), 7-21.
| Crossref | Google Scholar |

Dai W, Viraktamath CA, Zhang Y (2012) Ulopsina, a remarkable new ulopine leafhopper genus from China. Journal of Insect Science 12, 70.
| Crossref | Google Scholar | PubMed |

Dietrich CH (2005) Keys to the families of Cicadomorpha and subfamilies and tribes of Cicadellidae (Hemiptera: Auchenorrhyncha). Florida Entomologist 88(4), 502-517.
| Crossref | Google Scholar |

Dietrich CH, Rakitov RA, Holmes JL, Black WC (2001) Phylogeny of the major lineages of Membracoidea (Insecta: Hemiptera: Cicadomorpha) based on 28S rDNA sequences. Molecular Phylogenetics and Evolution 18(2), 293-305.
| Crossref | Google Scholar | PubMed |

Dietrich CH, Allen JM, Lemmon AR, Lemmon EM, Takiya DM, Evangelista O, Walden KKO, Grady PGS, Johnson KP (2017) Anchored hybrid enrichment-based phylogenomics of leafhoppers and treehoppers (Hemiptera: Cicadomorpha: Membracoidea). Insect Systematics and Diversity 1(1), 57-72.
| Crossref | Google Scholar |

Dietrich CH, Dmitriev DA, Takiya DM, Thomas MJ, Webb MD, Zahniser JN, Zhang Y (2022) Morphology-based phylogenetic analysis of Membracoidea (Hemiptera: Cicadomorpha) with placement of fossil taxa and description of a new subfamily. Insect Systematics and Diversity 6(5), 1-30 7.
| Crossref | Google Scholar |

Dmitriev DA (2010) Homologies of the head of Membracoidea based on nymphal morphology with notes on other groups of Auchenorrhyncha (Hemiptera). European Journal of Entomology 107, 597-613.
| Crossref | Google Scholar |

Emeljanov AF (1996) To the knowledge of leafhoppers of the family Ulopidae (Homoptera, Cicadina). Entomologicheskoe Obozrenie 75(2), 278-293.
| Google Scholar |

Encinas-Viso F, Bovill J, Albrecht DE, Florez‐Fernandez J, Lessard B, Lumbers J, Rodriguez J, Schmidt‐Lebuhn A, Zwick A, Milla L (2022) Pollen DNA metabarcoding reveals cryptic diversity and high spatial turnover in alpine plant–pollinator networks. Molecular Ecology 32, 6377-6393.
| Crossref | Google Scholar |

Evangelista O, Florez-V C, Sakakibara AM (2014) The identity of the treehopper genus Dysyncritus Fowler, with descriptions of new related taxa (Hemiptera: Membracidae: Heteronotinae). Zootaxa 3847(4), 495-532.
| Google Scholar |

Evans JW (1937) Australian Leafhoppers (Jassoidea: Homoptera) Part 4. — (Ledridae, Ulopidae and Euscelidae, Paradorydiini). Papers and Proceedings of the Royal Society of Tasmania 1936, 37-50.
| Google Scholar |

Evans JW (1939) Some new Australian Leafhoppers (Homoptera: Jassoidea). Transactions of the Royal Society of South Australia 63(1), 44-50.
| Google Scholar |

Evans JW (1947) Some new Ulopinae (Homoptera, Jassidae). Annals and Magazine of Natural History 14(11), 140-150.
| Google Scholar |

Evans JW (1951) Some notes on the classification of the leafhoppers (Jassoidea, Homoptera) with special reference to the Nearctic fauna. Commentationes Biologicae Societas Scientiarum Fennica 12, 1-11.
| Google Scholar |

Evans JW (1966) The leafhoppers and froghoppers of Australia and New Zealand (Homoptera: Cicadelloidea and Cercopoidea). Australian Museum Memoir 12, 1-347.
| Crossref | Google Scholar |

Evans JW (1968) Some relict New Guinea leaf hoppers and their significance in relation to the comparative morphology of the head and thorax of the Homoptera Auchenorrhyncha. Pacific Insects 10, 215-229.
| Google Scholar |

Evans JW (1977) The leafhoppers and froghoppers of Australia and New Zealand (Homoptera: Cicadelloidea and Cercopoidea). Part 2. Records of the Australian Museum 31(3), 83-129.
| Crossref | Google Scholar |

Fletcher MJ (2009) Identification keys and checklists for the leafhoppers, planthoppers and their relatives occurring in Australia and neighbouring areas (Hemiptera: Auchenorrhyncha). (New South Wales Government, Department of Primary Industries, Biosecurity Collections) Available at https://idtools.dpi.nsw.gov.au/keys/auch/index.html

Fletcher MJ (2012) Genus Austrolopa Evans, 1937. (Australian Faunal Directory. Australian Biological Resources Study: Canberra, ACT, Australia) Available at https://biodiversity.org.au/afd/taxa/Austrolopa

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644-652.
| Crossref | Google Scholar | PubMed |

Hamilton KGA (1983) Classification, morphology and phylogeny of the family Cicadellidae (Rhynchota: Homoptera) In ‘Proceedings of the 1st International Workshop on Biotaxonomy, Classification and Biology of Leafhoppers and Planthoppers of Economic Importance’, 4–7 October 1982, London, UK. (Eds WJ Knight, NC Pant, TS Robertson, MR Wilson) pp. 15–37. (Commonwealth Institute of Entomology: London, UK)

Hamilton KGA (1990) Chapter 6. Homoptera. In ‘Insects from the Santana Formation, Lower Cretaceous of Brazil’. (Ed. DA Grimaldi) Bulletin of the American Museum of Natural History, vol. 195, pp. 82–122. (American Museum of Natural History) Available at https://flow.hemiptera-databases.org/flowpdf/349.pdf

Harvey MS (2002) Short-range endemism amongst the Australian fauna: some examples from non-marine environments. Invertebrate Systematics 16(4), 555-570.
| Crossref | Google Scholar |

Hu Y, Dietrich CH, Skinner RK, Zhang Y (2023) Phylogeny of Membracoidea (Hemiptera: Auchenorrhyncha) based on transcriptome data. Systematic Entomology 48(1), 97-110.
| Crossref | Google Scholar |

Johnson KP, Dietrich CH, Friedrich F, Beutel RG, Wipfler B, Peters RS, Allen JM, Petersen M, Donath A, Walden KKO, Kozlov AM, Podsiadlowski L, Mayer C, Meusemann K, Vasilikopoulos A, Waterhouse RM, Cameron SL, Weirauch C, Swanson DR, Percy DM, Hardy NB, Terry I, Liu S, Zhou X, Misof B, Robertson HM, Yoshizawa K (2018) Phylogenomics and the evolution of hemipteroid insects. Proceedings of the National Academy of Sciences of the United States of America 115(50), 12775-12780.
| Crossref | Google Scholar | PubMed |

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar | PubMed |

Krueger F (2015) ‘Trim Galore! A wrapper around Cutadapt and FastQC to consistently apply adapter and quality trimming to FastQ files, with extra functionality for RRBS data.’ (Babraham Institute)

Krugner R, Sisterson MS, Backus EA, Burbank LP, Redak RA (2019) Sharpshooters: a review of what moves Xylella fastidiosa. Austral Entomology 58(2), 248-267.
| Crossref | Google Scholar |

Le SQ, Dang CC, Gascuel O (2012) Modeling protein evolution with several amino acid replacement matrices depending on site rates. Molecular Biology and Evolution 29(10), 2921-2936.
| Crossref | Google Scholar |

Leinonen R, Sugawara H, Shumway M, on behalf of the International Nucleotide Sequence Database Collaboration (2011) The sequence read archive. Nucleic acids research 39(suppl_1), D19-D21.
| Crossref | Google Scholar | PubMed |

Marsh JR, Bal P, Fraser H, Greenville A, Latty T, Moir ML, Rumpff L, Umbers K, Woinarski JC (2023) Impacts of the 2019–20 wildfires on Australian invertebrates. Australia’s Megafires: Biodiversity Impacts and Lessons from 2019–2020. Project 8.3.1, final report. (NESP Threatened Species Recovery Hub: Brisbane, Qld, Australia)

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530-1534.
| Crossref | Google Scholar | PubMed |

Moir ML, Majer JD, Fletcher MJ (2003) New records for Hemiptera species in Western Australia. Records of the Western Australian Museum 21(4), 353-357.
| Crossref | Google Scholar |

Rakitov RA (1996) Post-moulting behaviour associated with Malpighian tubule secretions in leafhoppers and treehoppers (Auchenorrhyncha: Membracoidea). European Journal of Entomology 93, 167-184.
| Google Scholar |

Rakitov RA (1998) On differentiation of cicadellid leg chaetotaxy (Homoptera: Auchenorrhyncha: Membracoidea). Russian Entomological Journal 6, 7-27.
| Google Scholar |

Rakitov RA, Godoy C (2005) New egg-powdering sharpshooters (Hemiptera: Cicadellidae: Proconiini) from Costa Rica. Annals of the Entomological Society of America 98(4), 444-457.
| Crossref | Google Scholar |

Rosauer D, Laffan SW, Crisp MD, Donnellan SC, Cook LG (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Molecular Ecology 18(19), 4061-72.
| Crossref | Google Scholar | PubMed |

Schmidt HA, Strimmer K, Vingron M, Von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18(3), 502-504.
| Crossref | Google Scholar | PubMed |

Skinner RK, Dietrich CH, Walden KKO, Gordon E, Sweet AD, Podsiadlowski L, Petersen M, Simon C, Takiya DM, Johnson KP (2019) Phylogenomics of Auchenorrhyncha (Insecta: Hemiptera) using transcriptomes: examining controversial relationships via degeneracy coding and interrogation of gene conflict. Systematic Entomology 45(1), 85-113.
| Crossref | Google Scholar |

Wang J-J, Wu Y-F, Yang M-F, Dai R-H (2020) The phylogenetic implications of the mitochondrial genomes of Macropsis notata and Oncopsis nigrofasciata. Frontiers in Genetics 11, 443.
| Crossref | Google Scholar |