Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

The Asian rock-dwelling antlions Gatzara Navás, 1915 and Nepsalus Navás, 1914 (Neuroptera: Myrmeleontidae): new advancements in systematics, biogeography and life history

Yuchen Zheng https://orcid.org/0000-0003-2397-2008 A , Yuezheng Tu https://orcid.org/0000-0001-5825-3391 A , Zuqi Mai https://orcid.org/0000-0003-3124-2021 B C , Davide Badano https://orcid.org/0000-0001-9715-3107 D * and Xingyue Liu https://orcid.org/0000-0002-9168-0659 A *
+ Author Affiliations
- Author Affiliations

A Department of Entomology, China Agricultural University, Beijing, 100193, PR China.

B Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, CZ-165 00 Prague‑Suchdol, Czechia.

C School of Agriculture, Sun Yat-sen University, Guangzhou, Guangdong, PR China.

D Department of Life Sciences, University of Siena, Via Aldo Moro 2, I-53100 Siena, Italy.


Handling Editor: Andy Austin

Invertebrate Systematics 38, IS24010 https://doi.org/10.1071/IS24010
Submitted: 24 January 2024  Accepted: 14 May 2024  Published: 19 June 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

The antlion genera Gatzara and Nepsalus (Myrmeleontidae: Dendroleontinae) inhabit mountain forests and are characterised by camouflaging larvae. Both genera remain poorly known despite recent findings on systematics and distribution. We report the discovery of new specimens and the previously unknown larvae of the rare species Gatzara jubilaea Navás, 1915, Nepsalus insolitus (Walker, 1860) and N. decorosus (Yang, 1988). These provide new evidence regarding the affinities of these species, and updated knowledge of the distribution, larval morphology and biology. Moreover, a new species of Nepsalus, N. maclachlani Badano, Zheng & Liu, sp. nov. is described from Sri Lanka based on historical museum collections. The discovery of the immature stages of Gatzara shows that the larvae of this genus share the same specialised ecological characteristics and habits as those of Nepsalus but are less morphologically derived. We also reconstruct a molecular phylogeny of this lineage, estimating the divergence time and biogeographical history by adding the new samples. The evolution of the Gatzara + Nepsalus lineage is associated with two major mountain ranges on the southern Tibetan Plateau, i.e. the Himalayas and the Hengduan Mountains.

ZooBank: urn:lsid:zoobank.org:pub:68E68211-DFC1-4D98-997B-8A23BA8F9B69

Keywords: Himalayas, historical biogeography, lacewing, larval morphology, oriental, palaearctic, phylogeny, taxonomy.

References

Ábrahám L, Giacomino M (2020) A little known and synonym ant-lions 2 (Neuroptera: Myrmeleontidae). Natura Somogyiensis 34, 21-72.
| Crossref | Google Scholar |

Acevedo F, Badano D, Monserrat VJ (2014) The larva of Tricholeon relictus Hölzel & Monserrat, 2002 a synanthropic antlion (Neuroptera, Myrmeleontidae). Zootaxa 3835, 364-370.
| Crossref | Google Scholar | PubMed |

Aspöck U, Aspöck H (2008) Phylogenetic relevance of the genital sclerites of Neuropterida (Insecta: Holometabola). Systematic Entomology 33, 97-127.
| Crossref | Google Scholar |

Baba K (1953) アリジゴクの生物誌. Journal: 越佐昆虫同好会会報臨時増刊 [‘The biology of antlions.’] (Essa Entomological Association: Niigata, Japan) [In Japanese]

Baba K, Edashige T (1954) コ英ダラウスバカゲロウの形態及び生態学的知見 [Morphological and ecological notes on Dendroleon jezoensis Okamoto (Neuroptera: Myrmeleonidae).]. 昆蟲 [Kontyû] 21, 51-59 [In Japanese].
| Google Scholar |

Badano D, Pantaleoni RA (2014a) The larvae of European Myrmeleontidae (Neuroptera). Zootaxa 3762, 1-71.
| Google Scholar |

Badano D, Pantaleoni RA (2014b) The Larvae of European Ascalaphidae (Neuroptera). Zootaxa 3796, 287-319.
| Google Scholar |

Badano D, Aspöck H, Aspöck U, Haring E (2017) Eyes in the dark … shedding light on the antlion phylogeny and the enigmatic genus Pseudimares Kimmins (Neuropterida: Neuroptera: Myrmeleontidae). Arthropod Systematics & Phylogeny 75, 535-554.
| Google Scholar |

Banks N (1929) Fauna of the Batu Caves, Selangor. xiii. Neuroptera. On the myrmeleonid Neglurus vitripennis Navás. Journal of the Federated Malay States Museums 14, 372-373.
| Google Scholar |

Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313-319.
| Crossref | Google Scholar | PubMed |

Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| Crossref | Google Scholar | PubMed |

Breitkreuz LCV, Winterton SL, Engel MS (2017) Wing tracheation in Chrysopidae and other Neuropterida (Insecta): a resolution of the confusion about vein fusion. American Museum Novitates 3890, 1-44.
| Crossref | Google Scholar |

Brower AV (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91, 6491-6495.
| Crossref | Google Scholar | PubMed |

Ding WN, Ree RH, Spicer RA, Xing YW (2020) Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science 369, 578-581.
| Crossref | Google Scholar | PubMed |

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

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797.
| Crossref | Google Scholar | PubMed |

Favre A, Päckert M, Pauls SU, Jähnig SC, Uhl D, Michalak I, Muellner-Riehl AN (2015) The role of the uplift of the Qinghai–Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews 90, 236-253.
| Crossref | Google Scholar | PubMed |

Folmer O, Black M, Hoeh W, Lutz R, 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.
| Google Scholar | PubMed |

Ge XH, Ma WP (2014) 中国区域大地构造学教程 [‘Course of regional tectonics in China.’] (地质出版社 [Geological Publishing House]: Beijing, PR China) [In Chinese]

Hayashi M (2013) Antlions (Neuroptera: Myrmeleontidae) of Shimane and West Tottori Prefectures, Japan. Bulletin of the Hoshizaki Green Foundation 16, 189-205.
| Google Scholar |

Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London – B. Biological Sciences 270, 313-321.
| Crossref | Google Scholar | PubMed |

Hebert PDN, Ratnasingham S, deWaard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London – B. Biological Sciences 270, S96-S99.
| Crossref | Google Scholar | PubMed |

Jacques FMB, Shi G, Su T, Zhou Z (2015) A tropical forest of the middle Miocene of Fujian (SE China) reveals Sino-Indian biogeographic affinities. Review of Palaeobotany and Palynology 216, 76-91.
| Crossref | Google Scholar |

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
| Crossref | Google Scholar | PubMed |

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, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649.
| Crossref | Google Scholar | PubMed |

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111-120.
| Crossref | Google Scholar | PubMed |

Krivokhatsky VA (1997) New and little known species of ant-lions (Neuroptera, Myrmeleontidae) from Indo-China. Entomological Review 76, 631-640.
| Google Scholar |

Krivokhatsky VA (2011) Муравьиные львы (Neuroptera: Myrmeleontidae) России [‘Antlions (Neuroptera: Myrmeleontidae) of Russia.’] (Товарищество Научных Изданий KMK [KMK Scientific Press]: Saint Petersburg, Russian Federation) [In Russian]

Kück P, Meusemann K (2010) FASconCAT: convenient handling of data matrices. Molecular Phylogenetics and Evolution 56, 1115-1118.
| Crossref | Google Scholar | PubMed |

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870-1874.
| Crossref | Google Scholar | PubMed |

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772-773.
| Crossref | Google Scholar | PubMed |

Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589-595.
| Crossref | Google Scholar | PubMed |

Machado RJP, Oswald JD (2020) Morphological phylogeny and taxonomic revision of the former antlion subtribe Periclystina (Neuroptera: Myrmeleontidae: Dendroleontinae). Zootaxa 4796, 1-322.
| Crossref | Google Scholar | PubMed |

Machado RJP, Gillung JP, Winterton SL, Garzón‐Orduña IJ, Lemmon AR, Lemmon EM, Oswald JD (2019) Owlflies are derived antlions: anchored phylogenomics supports a new phylogeny and classification of Myrmeleontidae (Neuroptera). Systematic Entomology 44, 418-450.
| Crossref | Google Scholar |

Mansell MW (1987) The ant-lions of southern Africa (Neuroptera: Myrmeleontidae): genus Cymothales Gerstaecker, including extralimital species. Systematic Entomology 12, 181-219.
| Crossref | Google Scholar |

Mansell MW (1988) The Myrmeleontidae (Neuroptera) of southern Africa: Genus Tricholeon Esben-Petersen. Neuroptera International 5, 45-55.
| Google Scholar |

Matsumoto R, Kikuta Y, Yoshitomi H (2016) Larvae of three Japanese species of Myrmeleontidae (Neuroptera). Japanese Journal of Systematic Entomology 22, 101-108.
| Google Scholar |

Matzke NJ (2014) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63, 951-970.
| Crossref | Google Scholar | PubMed |

Miller RB, Stange LA, Wang HY (1999) New species of antlions from Taiwan (Neuroptera: Myrmeleontidae). Journal of the National Taiwan Museum 52, 47-78.
| Google Scholar |

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the 2010 Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. INSPEC Accession Number 11705685. (IEEE) 10.1109/GCE.2010.5676129

Monserrat VJ (1985) Lista de los tipos de Mecoptera y Neuroptera (Insecta) de la colección L. Navás, depositados en el Museo de Zoología de Barcelona. Miscellània Zoològica 9, 233-243 [In Spanish].
| Google Scholar |

Navás L (1914) Myrméléonides (Ins. Névr.) nouveaux ou critiques [I]. Annales de la Société Scientifique de Bruxelles 38, 229-254 [In French].
| Google Scholar |

Navás L (1915) Neurópteros nuevos o poco conocidos (Cuarta [iv] serie). Memorias de la Real Academia de Ciencias y Artes de Barcelona 11, 373-398 [In Spanish].
| Google Scholar |

Navás L (1935) Neurópteros exóticos. 2.a serie. Memorias de la Real Academia de Ciencias y Artes de Barcelona 25, 37-59 [In Spanish].
| Google Scholar |

New TR (2003) ‘The Neuroptera of Malesia. Fauna Malesiana. Vol. 4.’ (Brill: Leiden, Netherlands)

Oswald JD (2023) Neuropterida species of the world: a catalogue and monograph of the species and subspecies of the extant and extinct Neuroptera, Megaloptera, Raphidioptera, and Glosselytrodea (Insecta: Neuropterida) of the World. Research Publication number 1. (Lacewing Digital Library, Texas A&M University: College Station, TX, USA) Available at http://lacewing.tamu.edu/SpeciesCatalog/Main [Verified 12 October 2023]

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Sekimoto S (2014) Review of Japanese Myrmeleontide (Neuroptera). Insecta Matsumurana 70, 1-87.
| Google Scholar |

Spicer RA, Su T, Valdes PJ, Farnsworth A, Wu FX, Shi GL, Spicer TEV, Zhou ZK (2020) Why ‘the uplift of the Tibetan Plateau’ is a myth? National Science Review 8, nwaa091.
| Crossref | Google Scholar | PubMed |

Stange LA (1976) Clasificacion catalogo mundial de la tribu Dendroleontini con la redescripcion del genero Voltor Navás. Acta Zoologica Lilloana 31, 261-320 [In Spanish].
| Google Scholar |

Stange LA (2004) A systematic catalog, bibliography and classification of the world antlions (Insecta: Neuroptera: Myrmeleontidae). Memoirs of the American Entomological Institute 74, 1-565.
| Google Scholar |

Stange LA (2008) A new species of the genus Dendroleon Brauer from Mexico (Neuroptera: Myrmeleontidae). Insecta Mundi 54, 1-9.
| Google Scholar |

Stange LA, Miller RB (2012) The cave mouth antlions of Australia (Neuroptera: Myrmeleontidae). Insecta Mundi 250, 1-65.
| Google Scholar |

Stange LA, Wang HY (1998) 認識台灣的昆蟲18: 脈翅目.廣翅目.蛇蛉目 [‘Guide book to insects in Taiwan. 18. Neuroptera, Megaloptera, Raphidioptera.’] (百通圖書股份有限公司 [Hsu Hsin Books Ltd. Co.]: Taiwan) [In Chinese]

Stange LA, Miller RB, Wang HY (2003) 臺灣的蟻蛉分類系統和生物學 [‘Identification and biology of Myrmeleontidae (Neuroptera) in Taiwan.’] (宜蘭縣自然史教育館 [I-Lan County Museum of Natural History]: Taiwan) [In Chinese]

Walker F (1860) XIII. Characters of undescribed Neuroptera in the Collection of W. W. Saunders, Esq., F.R.S., &c. Transactions of the Royal Entomological Society of London 10, 176-199.
| Crossref | Google Scholar |

Wang XL, Ao WG, Wang ZL, Wan X (2012) Review of the genus Gatzara Navás, 1915 from China (Neuroptera: Myrmeleontidae). Zootaxa 3408, 34-46.
| Crossref | Google Scholar |

Wang XL, Zhan QB, Wang AQ (2018) 中国动物志昆虫纲第六十八卷脉翅目蚁蛉总科 [‘Fauna Sinica, Insecta, Vol. 68, Neuroptera: Myrmeleontoidea.’] (科学出版社 [Science Press]: Beijing, PR China) [In Chinese]

Xu W, Dong WJ, Fu TT, Gao W, Lu CQ, Yan F, Wu YH, Jiang K, Jin JQ, Chen HM, Zhang YP, Hillis DM, Che J (2021) Herpetological phylogeographic analyses support a Miocene focal point of Himalayan uplift and biological diversification. National Science Review 8, nwaa263.
| Crossref | Google Scholar | PubMed |

Yang CK (1987) 脉翅目 [Neuroptera]. In 西藏农业病虫及杂草 [‘Agricultural insects, spiders, plant diseases and weeds of Xizang. Vol. 1’]. (Ed. SM Zhang) pp. 191–219. (西藏人民出版社 [Xizang Renmin Press House]: Xizang, PR China) [In Chinese]

Yang CK (1988) 脉翅目: 溪蛉科, 栉角蛉科, 褐蛉科, 草蛉科, 螳蛉科, 蚁蛉科, 蝶角蛉科, 粉蛉科 [Neuroptera: Osmylidae, Dilaridae, Hemerobiidae, Chrysopidae, Mantispidae, Myrmeleontidae, Ascalaphidae, Corydalidae]. In 西藏南迦巴瓦峰地区昆虫 [‘Insects of Mount Namjagbarwa region of Xizang’]. (Eds FS Huang, PY Wang, WY Yin, PY Yu, TS Lee, CK Yang, XJ Wang) pp. 193–216. (科学出版社 [Science Press]: Beijing, PR China) [In Chinese]

Yang CK (1997) 脉翅目: 蚁蛉科 [Neuroptera: Myrmeleonidae]. In 长江三峡库区昆虫 [‘Insects of the Three Gorge Reservoir area of Yangtze River. Vol. 1’]. (Ed. XK Yang) pp. 613–620. (重庆出版社 [Chongqing Publishing House]: Chongqing, PR China) [In Chinese]

Yang CK, Wang XL (2002) 脉翅目: 蚁蛉科 [Neuroptera: Myrmeleontidae]. In 海南森林昆虫 [‘Forest insects of Hainan’]. (Ed. FS Huang) pp. 296–299. (科学出版社 [Science Press]: Beijing, PR China) [In Chinese]

Yang D, Liu XY, Yang XK (2018) 中国生物物种名录第二卷动物昆虫 (II)脉翅总目 [‘Species Catalogue of China. Vol. 2, Animals, Insecta (II), Neuropterida.’] (科学出版社 [Science Press]: Beijing, PR China) [In Chinese]

Yu Y, Blair C, He XJ (2020) RASP 4: ancestral state reconstruction tool for multiple genes and characters. Molecular Biology and Evolution 37, 604-606.
| Crossref | Google Scholar | PubMed |

Zheng YC, Liu XY (2020) First description of immature stages of the antlion Bullanga florida (Navás, 1913) (Neuroptera, Myrmeleontidae, Dendroleontini). Zootaxa 4858, 394-404.
| Google Scholar |

Zheng YC, Hayashi F, Price BW, Liu XY (2022) Unveiling the evolutionary history of a puzzling antlion genus Gatzara Navás (Neuroptera: Myrmeleontidae: Dendroleontinae) based on systematic revision, molecular phylogenetics, and biogeographic inference. Insect Systematics and Diversity 6, 4.
| Crossref | Google Scholar |

Zheng YC, Badano D, Liu XY (2023) Systematic revision, molecular phylogeny and biogeography of the antlion tribe Acanthoplectrini (Neuroptera: Myrmeleontidae: Dendroleontinae), with emphasis on the Oriental lineage. Systematic Entomology 48(1), 40-68.
| Crossref | Google Scholar |

Zhu H, Tan YH (2022) Flora and vegetation of Yunnan, southwestern China: diversity, origin and evolution. Diversity 14, 340.
| Crossref | Google Scholar |

Zhu H, Chai Y, Zhou SS, Yan LC, Shi JP, Yang GP (2016) Combined community ecology and floristics, a synthetic study on the upper montane evergreen broad-leaved forests in Yunnan, southwestern China. Plant Diversity 38, 295-302.
| Crossref | Google Scholar | PubMed |