Eur. J. Entomol. 122: 42-55, 2025 | DOI: 10.14411/eje.2025.005

A general theory of the complex pronotum morphology of treehoppers in Smiliinae and its relatives (Hemiptera: Membracidae) and its applicability to other subfamiliesOriginal article

Kanta SUGIURA1, 2, Tensho TERANO1, Haruhiko ADACHI ORCID...3, Jin HAGIWARA3, Keisuke MATSUDA ORCID...3, Kenji NISHIDA ORCID...4, Paul HANSON ORCID...5, Shigeru KONDO ORCID...3, Yasuhiko CHIKAMI ORCID...1, Hiroki GOTOH ORCID...1, 2, *
1 Department of Biological Science, Faculty of Science, Shizuoka University, Shizuoka, Japan; e-mails: sugiura.kanta.19@shizuoka.ac.jp, 8891974141@edu.k.u-tokyo.ac.jp (TT), yasuhiko.chikami.evol@gmail.com, goto.hiroki@shizuoka.ac.jp
2 Department of Science, Graduate School of Integrated Science and Technology, Shizuoka University, Shizuoka, Japan
3 Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka, Japan; e-mails: hadachi@keio.jp, hagiwara.jin@fbs.osaka-u.ac.jp, kmatsudafbs@gmail.com, skondo@fbs.osaka-u.ac.jp
4 Associate Researcher, Museo de Zoología, Universidad de Costa Rica and Estación Biológica Monteverde, Monteverde, Puntarenas, Costa Rica; e-mail: kenji.nishida@gmail.com
5 Escuela de Biología, Universidad de Costa Rica, San Pedro de Montes de Oca, San José, Costa Rica; e-mail: phanson91@gmail.com

Treehoppers are characterized by exaggerated and three-dimensionally modified pronotal structures, known as "helmets". The treehopper pronotum has been studied mainly in terms of taxonomic diagnosis for over a century. It has recently been used as a model for studying the origin of evolutionary innovation and morphological diversification. However, the interspecific correspondence of traits, i.e., homology of pronotal parts, remains ambiguous due to (1) the extreme diversity in pronotal morphology and (2) little comparative study focused on homology. These problems hinder tracing the evolutionary history of treehopper pronotal morphology. Here, we investigate the homological relationships of pronotal structures among treehoppers, especially in the subfamily Smiliinae. We first investigate smiliine species, whose pronotal morphology is relatively simple, then expand to species with a more complex pronotum. Our comparative observations using six smiliine species reveal that four traits share the same positions and structures among these species: (1) the humeral angle, (2) the median carina, (3) the starting point of the median carina, and (4) the posterior apex of the pronotum, indicating that these traits are homologous across these species. Based on this homology hypothesis, we generalize the pronotal morphology and propose landmarks to help interpret the diversified pronotum of a clade including Smiliinae and its relatives. Finally, we confirm that this generalization can be applied to other treehopper subfamilies. Our homology-based approach can provide a strategy to recognize the trajectory of pronotal morphology, which is often difficult to trace.

Keywords: 3D structure, Centrotinae, Endoiastinae, homology, Membracinae, micro-CT, morphogenesis, pronotum, Stegaspidinae

Received: August 7, 2024; Revised: February 14, 2025; Accepted: February 14, 2025; Published online: February 25, 2025  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SUGIURA, K., TERANO, T., ADACHI, H., HAGIWARA, J., MATSUDA, K., NISHIDA, K., ... GOTOH, H. (2025). A general theory of the complex pronotum morphology of treehoppers in Smiliinae and its relatives (Hemiptera: Membracidae) and its applicability to other subfamilies. EJE, 122, Article 42-55. https://doi.org/10.14411/eje.2025.005
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Adachi H., Matsuda K., Nishida K., Hanson P., Kondo S. & Gotoh H. 2020: Structure and development of the complex pronotum of treehoppers (Insecta: Hemiptera: Membracidae). - Zool. Lett. 6: 3, 9 pp. Go to original source...
    2. Buckton G.B. & Poulton E.B. 1903: A Monograph of the Membracidae. Lovell Reeve & Company, London, 562 pp. Go to original source...
    3. Cryan J.R., Wiegmann B.M., Deitz L.L. & Dietrich C.H. 2000: Phylogeny of the treehoppers (Insecta: Hemiptera: Membracidae): Evidence from two nuclear genes. - Mol. Phylogenet. Evol. 17: 317-334. Go to original source...
    4. Dietrich C.H., Mckamey S.H. & Deitz L.L. 2001: Morphology-based phylogeny of the treehopper family Membracidae (Hemiptera: Cicadomorpha: Membracoidea). - Syst. Entomol. 26: 213-239. Go to original source...
    5. Dietrich C., Allen J., Lemmon A., Lemmon E., Takiya D., Evangelista O., Walden K., Grady P. & Johnson K. 2017: Anchored hybrid enrichment-based phylogenomics of leafhoppers and treehoppers (Hemiptera: Cicadomorpha: Membracoidea). - Insect Syst. Diversity 1: 57-72. Go to original source...
    6. Dmitriev D.A., Anufriev G.A., Bartlett C.R., Blanco-Rodríguez E., Borodin O.I., Cao Y.-H., Deitz L.L., Dietrich C.H., Dmitrieva M.O. et al. 2024: Membracidae Rafinesque, 1815. World Auchenorrhyncha Database. TaxonPages. URL: https://hoppers.speciesfile.org/otus/48812/overview (last accessed 11 June 2024).
    7. Evangelista O. & Sakakibara A.M. 2007: New species of the treehopper tribe Amastrini (Hemiptera, Membracidae, Smiliinae). - Rev. Bras. Entomol. 51: 38-41. Go to original source...
    8. Evangelista O., Sakakibara A.M., Cryan J.R. & Urban J.M. 2017a: A phylogeny of the treehopper subfamily Heteronotinae reveals convergent pronotal traits (Hemiptera: Auchenorrhyncha: Membracidae). - Syst. Entomol. 42: 410-428. Go to original source...
    9. Evengelista O., Flórez-V C., Takiya D.M., Cryan J.R., Dietrich C.H. & Urban J.M. 2017b: Molecular-based phylogeny of the treehopper family Membracidae: towords a revised classification of higher-level taxa. In Mejdalani G. & Felix M. (eds): Abstract Book, 15th International Auchenorrhyncha Congress, Mendes, RJ, Brazil, July 9-15, 2017. pp. 1222-1223
    10. Fisher C.R., Wegrzyn J.L. & Jockusch E.L. 2020: Co-option of wing patterning genes underlies the evolution of the treehopper pronotum. - Nat. Ecol. Evol. 4: 250-260. Go to original source...
    11. Flórez-V C. & Evangelista O. 2007: New species in the treehopper genus Bocydium Latreille, with description of nymphal stages and observations on their natural history. - Zootaxa 4281: 22-57. Go to original source...
    12. Flynn D.J. & Wheeler Jr. A.G. 2016: Micrutalis pallens Fowler (Hemiptera: Membracidae): First U.S. records, host-plant association, description of male, and redescription of female. - Proc. Entomol. Soc. Wash. 118: 345-353. Go to original source...
    13. Flynn D.J. 2019: Review of the genus Cladonota Stål with keys, illustrations of adults, and description of a new species from Ecuador (Hemiptera: Membracidae: Membracinae: Hypsoprorini). II. Subgenus Cladonota Stål. - Proc. Entomol. Soc. Wash. 121: 405-428. Go to original source...
    14. Godoy C., Miranda X. & Nishida K. 2006: Membrácidos de la América Tropical. Ediotrial INBio, Santo Domingo de Heredia, 352 pp.
    15. González-Mozo L.C. & Ware J.E. 2023: Review of Nasuconia Sakakibara, 2006 (Hemiptera: Membracidae) with description of three new species. - Zootaxa 5380: 321-340. Go to original source...
    16. McKamey S.H. 2023: Three new monobasic genera and three new species of the New World treehopper tribe Acutalini (Hemiptera, Membracidae, Smiliinae) with a key to all genera. - Zookeys 1143: 189-203. Go to original source...
    17. Miranda X. & Orlich-Ramírez C. 2024: Imaginal moulting behaviour in Ennya chrysura (Hemiptera: Membracidae), finding new questions and insights into the extreme morphology of treehoppers. - Anim. Behav. DOI: 10.1016/j.anbehav.2024.01.027 Go to original source...
    18. Owen R. 1843: Lectures on the Comparative Anatomy and Physiology of the Invertebrate Animals. Longman, Brown, Green & Longmans, London, 392 pp. Go to original source...
    19. Plummer C.C. 1945: New Membracidae from Central America. - Proc. Entomol. Soc. Wash. 47: 39-44.
    20. Remane A. 1952: Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. Akademische Verlagsgesellschaft, Leipzig, 400 pp.
    21. Stegmann U.E. 1998: An exaggerated trait in insects: the prothoracic skeleton of Stictocephala bisonia (Homoptera: Membracidae). - J. Morphol. 238: 157-178. Go to original source...
    22. Sugiura K., Terano T., Adachi H., Hagiwara J., Matsuda K., Nishida K., Paul H., Kondo S. & Gotoh H. 2024: Histological observation of pronotum development in the treehopper Poppea capricornis (Insecta: Hemiptera: Membracidae). - Zool. Sci. 41: 167-176. Go to original source...
    23. Wagner G.P. 1989: The biological homology concept. - Annu. Rev. Ecol. Syst. 20: 51-69. Go to original source...
    24. Wake D.B. 2003: Homology and homoplasy. In Hall B.K. & Olson W.M. (eds): Keywords and Concepts in Evolutionary Developmental Biology, Harvard University Press, London, pp. 191-201. Go to original source...
    25. Wallace M.S. 2011: Morphology-based phylogenetic analysis of the treehopper tribe Smiliini (Hemiptera: Membracidae: Smiliinae), with reinstatement of the tribe Telamonini. - Zootaxa 3047(3047): 1-42. Go to original source...
    26. Wood T.K. 1993: Diversity in the new world Membracidae. - Annu. Rev. Entomol. 38: 409-433. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content