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Issue: Vol. 5621 No. 5: 22 Apr. 2025
Type: Article
Published: 2025-04-22
DOI: 10.11646/zootaxa.5621.5.3
Page range: 547-559
Abstract views: 128
PDF downloaded: 6

DNA-barcoding and ecological niche analysis of Wart Biters (Decticus spp.) from an endemism hotspot (Tettigoniidae: Tettigoniinae)

Istituto di Ricerca sugli Ecosistemi Terrestri IRET, Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, 50019 Sesto Fiorentino (Firenze), Italy. National Biodiversity Future Center, 90133 Palermo, Italy.
Department of Ecological and Biological Sciences, University of Tuscia, Viterbo, Italy.
Istituto di Ricerca sugli Ecosistemi Terrestri IRET, Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, 50019 Sesto Fiorentino (Firenze), Italy.
Istituto sull’Inquinamento Atmosferico (CNR – IIA), Consiglio Nazionale Delle Ricerche, Bari, Italy.
Department of Biology and Biotechnologies “Charles Darwin”, La Sapienza University of Rome, Rome, Italy.
Department of Science, Roma Tre University, Rome, Italy.
Via Palmiro Togliatti, 50019, Sesto Fiorentino (Firenze), Italy.
Department of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, Italy.
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, CNRS, IRD, EPHE, Montpellier, France.
Istituto di Ricerca sugli Ecosistemi Terrestri IRET, Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, 50019 Sesto Fiorentino (Firenze), Italy. National Biodiversity Future Center, 90133 Palermo, Italy.
Istituto di Ricerca sugli Ecosistemi Terrestri IRET, Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, 50019 Sesto Fiorentino (Firenze), Italy.
Orthoptera DNA-barcoding endemic species flightlessness

Abstract

Understanding biogeographical patterns is a challenging task, particularly in the case of poorly studied organisms, whose phylogenetic affinities and ecological needs are not yet understood. Such a case is common among invertebrates and particularly among insects, whose extensive diversity may hamper full and deep comprehension of their ecological and evolutionary patterns. Within insects, orthopterans also represent a relatively poorly studied group. Building knowledge upon biogeography and evolution of orthopterans may provide key insights to their conservation, especially in the case of range-restricted taxa that are inherently more vulnerable, and prone to extinction. In this study we thus applied an integrated approach, combining DNA-barcoding and ecological niche modelling, for investigating the diversity of wart biters (Orthoptera Tettigoniidae, genus Decticus). We particularly aimed at providing a first screening of the molecular identity of species within the genus, and an assessment of their macro-ecological needs. We analysed mitochondrial DNA (cytochrome oxidase I COI) and bioclimatic niche data for the four Decticus species that occur in the Italian Peninsula (D. verrucivorus, D. albifrons, D. loudoni, and D. aprutianus), reconstructing their phylogenetic relationships based on molecular approaches, and comparing their ecological preferences. We provide COI sequences for all the species found in Italy, including the first one available for two endemic ones. We found a clear molecular differentiation among the four species, with D. albifrons being the most distinct and basal taxon, as based on the COI sequence adopted. Our results also bring evidence of significant ecological niche differentiation, with each species occupying a distinct portion of the climatic space available within Italy. Notably, the two range-restricted and short-winged species, D. loudoni and D. aprutianus, result as sister taxa according to COI, and exhibit greater ecological specialisation compared to the more widespread species. Besides, we also highlight significant intra-taxon diversity for both D. verrucivorus sensu stricto and D. albifrons, suggesting that further research on potential intraspecific variability may be needed to clarify the taxonomic position of Italian populations. The observed genetic divergence and ecological niche differentiation found among wart biters suggest that adaptation to different ecological conditions may have played a role in the diversification of these range-restricted species. Our results confirmed the importance of the Italian Peninsula as a biodiversity hotspot for Orthoptera and provide a solid baseline for more in-depth molecular studies, besides providing novel sequences that may be used for e.g., DNA metabarcoding or eDNA campaigns. Further research is in fact needed to explore the specific ecological factors driving niche differentiation in this and other taxa, and to investigate the evolutionary pathways that led to the genus’ current diversity and distribution.

References

  1. Amori, G. & Castiglia, R. (2018) Mammal endemism in Italy: a review. Biogeographia, 3, 19–31. https://doi.org/10.21426/B633035335
  2. Ancillotto, L., Viviano, A., Baratti, M., Sogliani, D., Ladurner, E. & Mori, E. (2023) Every branch in its niche: intraspecific variation in habitat suitability of a widely distributed small mammal, the harvest mouse Micromys minutus. Mammal Research, 68, 575–585. https://doi.org/10.1007/s13364-023-00693-3
  3. Ancillotto, L. & Labadessa, R. (2024) Functional traits drive the fate of Orthoptera in urban areas. Insect Conservation and Diversity, 17, 304–311. https://doi.org/10.1111/icad.12683
  4. Basille, M., Calenge, C., Marboutin, É., Andersen, R. & Gaillard, J.M. (2008) Assessing habitat selection using multivariate statistics: Some refinements of the ecological-niche factor analysis. Ecological Modelling, 211, 233–240. https://doi.org/10.1016/j.ecolmodel.2007.09.006
  5. Bogdanowicz, W., Hulva, P., Černá Bolfíková, B., Buś, M.M., Rychlicka, E., Sztencel-Jabłonka, A., Cistrone, L. & Russo, D. (2015) Cryptic diversity of Italian bats and the role of the Apennine refugium in the phylogeography of the western Palaearctic. Zoological Journal of the Linnean Society, 174, 635–648. https://doi.org/10.1111/zoj.12248
  6. Carne, C. (2017) Predicting habitat suitability for the wart-biter bush cricket (Decticus verrucivorus) in Europe. Journal of Insect Conservation, 21, 287–295. https://doi.org/10.1007/s10841-017-9975-1
  7. Canestrelli, D., Cimmaruta, R. & Nascetti, G. (2008) Population genetic structure and diversity of the Apennine endemic stream frog, Rana italica–insights on the Pleistocene evolutionary history of the Italian peninsular biota. Molecular Ecology, 17, 3856–3872. https://doi.org/10.1111/j.1365-294X.2008.03870.x
  8. Ceccolini, F., Pizzocaro, L. & Cianferoni, F. (2020) New records of Orthoptera from Molise (Southern Italy) with an updated provisional checklist. Fragmenta Entomologica, 52, 85–99. https://doi.org/10.13133/2284-4880/416
  9. Cherrill, A.J. & Brown, V.K. (1990) The habitat requirements of adults of the Wart-biter Decticus verrucivorus (L.) (Orthoptera: Tettigoniidae) in Southern England. Biological Conservation, 53, 145–157. https://doi.org/10.1016/0006-3207(90)90005-A
  10. Cherrill, A.J. & Brown, V.K. (1992) Variation in body size between heathland and chalk grassland populations of the bush-cricket, Decticus verrucivorus (L.) (Orthoptera: Tettigoniidae), in southern England. Entomologist’s Gazette, 43, 77–82.
  11. Curto, J.D. & Pinto, J.C. (2011) The corrected vif (cvif). Journal of Applied Statistics, 38, 1499–1507. https://doi.org/10.1080/02664763.2010.505956
  12. Dapporto, L. (2010) Speciation in Mediterranean refugia and post‐glacial expansion of Zerynthia polyxena (Lepidoptera, Papilionidae). Journal of Zoological Systematics and Evolutionary Research, 48, 229–237. https://doi.org/10.1111/j.1439-0469.2009.00550.x
  13. DeMiguel, D. (2016) Disentangling adaptive evolutionary radiations and the role of diet in promoting diversification on islands. Scientific Reports, 6, 29803. https://doi.org/10.1038/srep29803
  14. Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315.
  15. 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 Biotechnology, 3, 294–299.
  16. Fontana, P., Odè, B. & Malagnini, V. (1999) On the identity of Decticus loudoni Ramme, 1933 (Insecta Orthoptera Tettigoniidae). Bollettino dell’Istituto di Entomologia “Giulio Grandi” dell’Università degli Studi di Bologna, 53, 71–85.
  17. Glor, R.E. (2010) Phylogenetic insights on adaptive radiation. Annual Review of Ecology, Evolution, and Systematics, 41, 251–270. https://doi.org/10.1146/annurev.ecolsys.39.110707.173447
  18. Götz, W. (1970) Zur Gröbenvariation im Formenkreis Decticus verrucivorus (Orthoptera, Saltatoria, Tettigoniidae). Zoologische Abhandlungen Museum Tierkunde Dresden, 31, 139–191.
  19. Homburg, K., Brandt, P., Drees, C. & Assmann, T. (2014) Evolutionarily significant units in a flightless ground beetle show different climate niches and high extinction risk due to climate change. Journal of Insect Conservation, 18, 781–790. https://doi.org/10.1007/s10841-014-9685-x
  20. Huemer, P., Mutanen, M., Sefc, K.M. & Hebert, P.D. (2014) Testing DNA barcode performance in 1000 species of European Lepidoptera: large geographic distances have small genetic impacts. PLos One, 9, e115774. https://doi.org/10.1371/journal.pone.0115774
  21. Iorio, C., Scherini, R., Fontana, P., Buzzetti, F.M., Kleukers, R., Odè, B. & Massa, B. (2019) Grasshoppers and crickets of Italy. A photographic field guide to all species. WBA Handbooks Editions, Verona, Italy.
  22. Kassen, R., Llewellyn, M. & Rainey, P.B. (2004) Ecological constraints on diversification in a model adaptive radiation. Nature, 431, 984–988. https://doi.org/10.1038/nature02923
  23. Koot, E.M., Morgan-Richards, M. & Trewick, S.A. (2022) Climate change and alpine-adapted insects: modelling environmental envelopes of a grasshopper radiation. Royal Society Open Science, 9, 211596. https://doi.org/10.1098/rsos.211596
  24. Labadessa, R. & Ancillotto, L. (2022) A tale of two crickets: global climate and local competition shape the distribution of European Oecanthus species (Orthoptera, Gryllidae). Frontiers of Biogeography, 14, e57538. https://doi.org/10.21425/F5FBG57538
  25. Löffler, F., Poniatowski, D. & Fartmann, T. (2019) Orthoptera community shifts in response to land-use and climate change–Lessons from a long-term study across different grassland habitats. Biological Conservation, 236, 315–323. https://doi.org/10.1016/j.biocon.2019.05.058
  26. Massa, B. (2013) Importanza della bioacustica nella sistematica degli Ortotteri. Atti Accademia nazionale Italiana di Entomologia, 61, 33–41.
  27. Massa, B. & Fontana, P. (2020) Endemism in Italian Orthoptera. Biodiversity Journal, 11, 405–434. https://doi.org/10.31396/Biodiv.Jour.2020.11.2.401.434
  28. Mattoccia, M., Marta, S., Romano, A. & Sbordoni, V. (2011) Phylogeography of an Italian endemic salamander (genus Salamandrina): glacial refugia, postglacial expansions, and secondary contact. Biological Journal of the Linnean Society, 104, 903–992. https://doi.org/10.1111/j.1095-8312.2011.01747.x
  29. McCulloch, G.A., Foster, B.J., Dutoit, L., Harrop, T.W., Guhlin, J., Dearden, P.K. & Waters, J.M. (2021) Genomics reveals widespread ecological speciation in flightless insects. Systematic Biology, 70, 863–876. https://doi.org/10.1093/sysbio/syaa094
  30. Menchetti, M., Talavera, G., Cini, A., Salvati, V., Dincă, V., Platania, L., Bonelli, S., Balletto, E., Vila, R. & Dapporto, L. (2021) Two ways to be endemic. Alps and Apennines are different functional refugia during climatic cycles. Molecular Ecology, 30, 1297–1310. https://doi.org/10.1111/mec.15795
  31. Mori, E., Nerva, L. & Lovari, S. (2019) Reclassification of the serows and the gorals: the end of a neverending story? Mammal Review, 49, 256–262. https://doi.org/10.1111/mam.12154
  32. Mori, E., Ancillotto, L., Viviano, A., Sogliani, D., Amori, G., Vella, F., Boano, G., Bertolino, S. & Monti, F. (2024) Anthropogenic dispersal explains the phylogeography of insular edible dormouse Glis glis in the Mediterranean basin. Mammal Research, 69, 401–410. https://doi.org/10.1007/s13364-024-00754-1
  33. Naimi, B. & Araujo, M.B. (2016) SDM: a reproducible and extensible R platform for species distribution modelling. Ecography, 39, 368–375. https://doi.org/10.1111/ecog.01881
  34. Panhwar, W.A., Sultana, R. & Wagan, M.S. (2017) Taxonomy of genus Decticus Serville, 1831 (Decticinae: Tettigoniidae: Orthoptera). Journal of Entomology and Zoology Studies, 5, 1100–1104.
  35. Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595–609. https://doi.org/10.1080/10635150600852011
  36. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
  37. Reis, T.S., Ciampi‐Guillardi, M., Bajay, M.M., de Souza, A.P. & Dos Santos, F.A.M. (2015) Elevation as a barrier: genetic structure for an Atlantic rain forest tree (Bathysa australis) in the Serra do Mar mountain range, SE Brazil. Ecology and Evolution, 5, 1919–1931. https://doi.org/10.1002/ece3.1501
  38. Ribeiro Leite, L.A. (2012) Mitochondrial pseudogenes in insect DNA barcoding: differing points of view on the same issue. Biota Neotropica, 12, 301–308. https://doi.org/10.1590/S1676-06032012000300029
  39. Rinnan, D.S. & Lawler, J. (2019) Climate‐niche factor analysis: a spatial approach to quantifying species vulnerability to climate change. Ecography, 42, 1494–1503. https://doi.org/10.1111/ecog.03937
  40. Rundle, H.D. & Nosil, P. (2005) Ecological speciation. Ecology Letters, 8, 336–352. https://doi.org/10.1111/j.1461-0248.2004.00715.x
  41. Salces-Castellano, A., Andújar, C., López, H., Pérez-Delgado, A.J., Arribas, P. & Emerson, B.C. (2021) Flightlessness in insects enhances diversification and determines assemblage structure across whole communities. Proceedings of the Royal Society B, 288, 20202646. https://doi.org/10.1098/rspb.2020.2646
  42. Samways, M.J. & Harz, K. (1982) Biogeography of intraspecific morphological variation in the bush crickets Decticus verrucivorus (L.) and D. albifrons (F.) (Orthoptera: Tettigoniidae). Journal of Biogeography, 9, 243–254.
  43. Samways, M.J. & Lockwood, J.A. (1998) Orthoptera conservation: pests and paradoxes. Journal of Insect Conservation, 2, 143–149.
  44. Schluter, D. (2009) Evidence for ecological speciation and its alternative. Science, 323, 737–741. https://doi.org/10.1126/science.1160006
  45. Sergeev, M.G., Molodtsov, V.V. & Storozhenko, S.Y. (2023) New data on distribution of Decticus nigrescens Tarbinsky, 1930 (Orthoptera: Tettigoniidae) in Russia. Far Eastern Entomologist, 487, 21–28.
  46. Serville, J.G.A. (1838) Decticus monspeliensis Rambur, 1838. In: Serville, J.G.A. (Ed.), Histoire naturelle des insectes. Orthoptères. Librairie Encyclopédique de Roret Editions, Paris, pp. 1–776.
  47. Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America, 105, 13486–13491. https://doi.org/10.1073/pnas.0803076105
  48. Stankowski, S. & Ravinet, M. (2021) Defining the speciation continuum. Evolution, 75, 1256–1273. https://doi.org/10.1111/evo.14215
  49. Stoch, F. (2000) How many endemic species? Species richness assessment and conservation priorities in Italy. Belgian Journal of Entomology, 2, 125–133. https://doi.org/10.1111/evo.14215
  50. Stolyarov, M.V. (2005) New data on distribution and taxonomy of the Orthoptera from Caucasus. 1. Stenopelmatoidea and Tettigonioideа. Proceedings of the Russian Entomological Society, San Petersburg, 76, 62–71.
  51. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120
  52. Tienstra, R.T. (1993) Dimensions in two coastal populations of the wartbiter (Decticus verrucivorus (L.)) in relation to biotope. Nieuwsbrief Saltabel, 9, 13–16.
  53. Ton, L., Morin, D., Foucart, A., Catil, J.M. & Nabholz, B. (2023) Le Dectique verrucivore, Decticus verrucivorus (Linnaeus, 1758), en France continentale: étude morphologique et implications taxonomiques (Orthoptera: Tettigoniidae). Materiaux Orthopteriques et Entomocenotiques, 28, 45–68.
  54. Vences, M., Miralles, A., Brouillet, S., Ducasse, J., Fedosov, A., Kharchev, V., Kostadinov, I., Kumari, S., Padmanidis, S., Scherz, M.D., Puillandre, N. & Renner, S.S. (2021) iTaxoTools 0.1: Kickstarting a specimen-based software toolkit for taxonomists. Megataxa, 6, 77–92. https://doi.org/10.11646/megataxa.6.2.1
  55. Vences, M., Patmanidis, S., Schmidt, J.C., Matschiner, M., Miralles, A. & Renner, S.S. (2024) Hapsolutely: a user-friendly tool integrating haplotype phasing, network construction and haploweb calculation. Bioinformatics Advances, 4, vbae083. https://doi.org/10.1093/bioadv/vbae083
  56. Voje, K.L., Hemp, C., Flagstad, Ø., Saetre, G.P. & Stenseth, N.C. (2009) Climatic change as an engine for speciation in flightless Orthoptera species inhabiting African mountains. Molecular Ecology, 18, 93–108. https://doi.org/10.1111/j.1365-294X.2008.04002.x
  57. Warheit, K.I., Forman, J.D., Losos, J.B. & Miles, D.B. (1999) Morphological diversification and adaptive radiation: a comparison of two diverse lizard clades. Evolution, 53, 1226–1234. https://doi.org/10.1111/j.1365-294X.2008.04002.x
  58. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876. https://doi.org/10.1093/bioinformatics/btt499

How to Cite

Ancillotto, L., Serafini, E., Viviano, A., Labadessa, R., Martino, J., Annessi, M., Bruni, G., Repetto, E., Nabholz, B., Mori, E. & Baratti, M. (2025) DNA-barcoding and ecological niche analysis of Wart Biters (Decticus spp.) from an endemism hotspot (Tettigoniidae: Tettigoniinae). Zootaxa, 5621 (5), 547–559. https://doi.org/10.11646/zootaxa.5621.5.3