Taxonomy of the Iberian species of Pseudochelidura (Dermaptera: Forficulidae)
Abstract
Male cerci variability was used as the main source of information to separate taxonomic units in the genus Pseudochelidura. Based on these data it was considered that three species of Pseudochelidura coexisted in the Pyrenees: P. sinuata, P. minor and P. montuosa. However, our phylogeographic and phylogenetic analyses based on molecular data (mitochondrial cytb and nuclear ITS2) do not support those conclusions. Combining these analyses with morphological studies we concluded that: 1) the Pyrenees are inhabited by a single evolutionary unit: P. sinuata (Germar, 1825) (= P. minor Steinmann, 1979 syn. nov., = P. montuosa Steinmann, 1981 syn. nov.). 2) Cantabrian and Pyrenean populations are reciprocally monophyletic and morphologically diagnosable representing two independent evolutionary units: Pseudochelidura cantabrica Cuesta-Segura, Jurado-Angulo & García-París sp. nov. and P. sinuata. And, 3) their conservation status needs to be evaluated in the light of current taxonomic changes. We have shown that the use of male cerci for species identification is problematic. Patterns of variation possibly affected by sexual selection (e.g., intrapopulational variability) appear to be very difficult to separate from variation driven by natural selection or genetic drift (i.e., character divergence in geographical isolation). The large sequence divergence observed between Pyrenean and Cantabrian populations of Pseudochelidura suggest a lasting genetic and geographic isolation between them, rendering difficult to ascertain their phylogenetic relationships.
References
Albouy V. 1984. Liste des dermaptères des collections du MNHN (Paris), suivie de quelques éléments de bibliographie (Dermaptera). Entomologica Gallica 1: 169–185.
Albouy V. & Caussanel C. 1990. Dermaptères et Perce-oreilles. Faune de France n° 75, Fédération Française des Sociétés de Sciences Naturelles, Paris.
Anlaş S. & Kočárek P. 2012. Current status of Dermaptera (Insecta) fauna of Turkey and Cyprus. Turkish Journal of Entomology 36 (1): 43–58.
Arribas O.J. 1999. Phylogeny and relationships of the Mountain lizards of Europe and Near East (Archaeolacerta Mertens, 1921 sensu lato) and their relationships among the Eurasian lacertid radiation. Russian Journal of Herpetology 6 (1): 1–22.
Arribas O.J., Carranza S. & Odierna G. 2006. Description of a new endemic species of mountain lizard from Northwestern Spain: Iberolacerta galani sp. nov.(Squamata: Lacertidae). Zootaxa 1240 (1): 1–55. https://doi.org/10.11646/zootaxa.1240.1.1
Bivar de Sousa A. 1997. Dermápteros (Insecta: Dermaptera) novos ou pouco conhecidos para Portugal Continental. Boletim da Sociedade Portuguesa de Entomologia 6 (17): 229–241.
Borelli A. 1905. Sur quelques forficules des Pyrénées. La Feuille des Jeunes Naturalistes série IV 35: 49–51.
de Bormans A. & Krauss H. 1900. Forficulidae und Hemimeridae. Das Tierreich 11, R. Friedländer und Sohn, Berlin. Available from https://www.biodiversitylibrary.org/page/43101643#page/11/mode/1up [accessed 3 Feb. 2023].
Burr M. 1915. On the male genital armature of the Dermaptera. I: Protodermaptera (except Psalidae). Journal of the Royal Microscopical Society 35 (5): 413–447. https://doi.org/10.1111/j.1365-2818.1915.tb04967.x
Caussanel C., Albouy V. & Cloupeau R. 1990. Un dermaptère nouveau pour la France, Pseudochelidura montuosa Steinmann, 1981. Les problèmes posés par le genre [Derm. Forficulidae]. Bulletin de la Société entomologique de France 95: 175–181. https://doi.org/10.3406/bsef.1990.17650
Chopard L. 1951. Orthoptéroïdes. Faune de France, 56, Paul Lechevalier, Paris.
Crochet P.A., Chaline O., Surget-Groba Y., Debain C. & Cheylan M. 2004. Speciation in mountains: phylogeography and phylogeny of the rock lizards genus Iberolacerta (Reptilia: Lacertidae). Molecular Phylogenetics and Evolution 30 (3): 860–866. https://doi.org/10.1016/j.ympev.2003.07.016
Cuesta-Segura A.D. 2012. Descubrimiento de Pseudochelidura minor (Steinmann, 1979) (Dermaptera: Forficulidae) en la Cordillera Cantábrica (noroeste de la Península Ibérica). Boletín de la Sociedad entomológica Aragonesa 50: 512.
Cuesta-Segura A.D. 2016. Respuesta de las Comunidades de Artrópodos a las Perturbaciones y a los Cambios en la Estructura de la Vegetación en Ecosistemas de Matorral de la Cordillera Cantábrica. PhD thesis, Universidad de León, España.
Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
Desmarest A.G. 1820. Faune française, ou Histoire naturelle, générale et particulière des animaux qui se trouvent en France, constamment ou passagèrement, à la surface du sol, dans les eaux qui le baignent, et dans le lit. Insectes Orthoptères. Chez Rapet, Paris.
Diakonov D.M. 1925. Experimental and biometrical investigations on dimorphic variability of Forficula. Journal of Genetics 15: 201–232. https://doi.org/10.1007/BF02983107
Dohrn H. 1867. Versuch einer Monographie der Dermapteren. Entomologische Zeitung 28 (7–9): 341–343. Available from https://www.biodiversitylibrary.org/page/33831408 [accessed 11 Jan. 2023].
Dubrony A. 1878. Liste des Orthoptères recueillis jusqu’ici en Ligurie. Annali del Museo Civico di Storia Naturale di Genova 12: 5–25.
Dufresnes C., Nicieza A.G., Litvinchuk S.N., Rodrigues N., Jeffries D.L., Vences M., Perrin N. & Martínez-Solano Í. 2020 Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs. Molecular Ecology 29 (5): 986–1000. https://doi.org/10.1111/mec.15368
Fabricius J.C. 1775. Systema entomologiae sistens insectorvm classes, ordines, genera, species, adiectis synonymis, locis, descriptionibvs, observationibvs. Kortius, Flensburg and Leipzig. https://doi.org/10.5962/bhl.title.36510
Fieber F.X. 1853. Synopsis der europäischen Orthopteren. Lotos. Zeitschrift für Naturwissenschaften 3: 252–258.
Finot A. 1887. Description de Forficula lesnei. Annales de la Société entomologique de France, Bulletin entomologique: clxxxix–cxc. Available from https://www.biodiversitylibrary.org/page/8231281 [accessed 11 Jan. 2023].
Fischer von Waldheim G. 1846. Entomographie Rossicae IV: Orthoptera Imperii Rossici. Nouveaux mémoires de la Société Impériale des naturalistes de Moscou 8. Available from https://www.biodiversitylibrary.org/page/54252057 [accessed 11 Jan. 2023].
Fontana P. 1999. The type specimens of Forficula described by Gené in 1832, at present belonging to the genus Chelidura Latreille, 1825 (Insecta Dermaptera). Bollettino del Museo Regionale di Scienze Naturali Torino 16: 127–150.
Fontana P., Buzzetti F.M., Cogo A. & Odé B. 2002. Guida al Riconoscimento e allo Studio di Cavallette, Grilli, Mantidi e Insetti affini del Veneto. Museo Naturalistico Archeologico di Vicenza.
Fontana P., Marangoni F., Kočárek P., Tirello P., Giovagnoli G. & Colacurcio L. 2021a. Updated knowledge on Italian Dermaptera with the report of a new alien species: Forficula smyrnensis Audinet-Serville, 1838. Memorie della Società Entomologica Italiana 97: 261–270. Available from http://hdl.handle.net/10449/68208 [accessed 11 Jan. 2023].
Fontana P., Pedrazzoli P., Malagnini V., Ruzzier E., Marangoni F. & Kočárek P. 2021b. Toward a revision of the genus Chelidura Latreille, 1825: designation of the Neotype for Chelidura aptera (Megerle in Charpentier, 1825) (Dermaptera: Forficulidae). Memorie della Società Entomologica Italiana 97: 279–302. https://doi.org/10.4081/memoriesei.2020.279
García-París M. 2017. Taxonomy of Iberian Anisolabididae (Dermaptera). Acta Zoologica Academiae Scientiarum Hungaricae 63: 29–43. https://doi.org/10.17109/AZH.63.1.29.2017
García-París M., Jurado-Angulo P., Martínez-Pérez S. & Micó E. 2021. Rediscovery of Forficula iberica Steinmann, 1981 (Dermaptera: Forficulidae). Zootaxa 5039 (2): 241–251. https://doi.org/10.11646/zootaxa.5039.2.5
Gené G. 1832. Saggio di una Monografia delle Forficule indigene. Annali delle Scienze del Regno Lombardo-Veneto 2: 215–228.
Gené G. 1833. Descrizione di una nuova Forficula italiana. Annali delle Scienze del Regno Lombardo-Veneto 3: 188–189.
Germar E.F. 1825. Fauna insectorum Europae. Fasciculus 11. Kümmel, Halle a.S. [Halae], 25 pls. https://doi.org/10.5962/bhl.title.127926
González-Miguéns R., Muñoz-Nozal E., Jiménez-Ruiz Y., Mas-Peinado P., Ghanavi H.R. & García-París M. 2020. Speciation patterns in the Forficula auricularia species complex: cryptic and not so cryptic taxa across the western Palaearctic region. Zoological Journal of the Linnean Society 190 (3): 788–823. https://doi.org/10.1093/zoolinnean/zlaa070
Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–8.
Harz K. & Kaltenbach A. 1976. Die Orthopteren Europas III – The Orthoptera of Europe III. W. Junk, The Hague. https://doi. org/10.1007/978-94-017-2513-2
Herrera Mesa L. 1999. Catálogo de los Dermápteros de España. Newbook, Navarra.
Herrich-Schäffer G.A. 1840. Nomenclator entomologicus: Verzeichniss der europäischen Insecten; zur Erleichterung des Tauschverkehrs mit Preisen versehen. Zweites Heft. Coleoptera, Orthoptera, Dermatoptera und Hymenoptera. Pustet, Regensburg. https://doi.org/10.5962/bhl.title.34052
Hewitt G.M. 1999. Postglacial re-colonization of European biota. Biology of the Linnean Society 68: 87–112. https://doi.org/10.1111/j.1095-8312.1999.tb01160.x
Hincks W. 1935. A note on the genus Lithinus Burr (Dermaptera). Entomologist‘s Monthly Magazine 71: 274–277.
Ji Y.J., Zhang D.X. & He J.J. 2003. Evolutionary conservation and versatility of a new set of primers for amplifying the ribosomal internal transcribed spacer regions in insects and other invertebrates. Molecular Ecology Notes 3: 581–585. https://doi.org/10.1046/j.1471-8286.2003.00519.x
Jurado-Angulo P., Jiménez-Ruiz Y. & García-París M. 2021. The Pyrenean species of Chelidura (Dermaptera, Forficulidae). Deutsche Entomologische Zeitschrift 68: 235–248. https://doi.org/10.3897/dez.68.68020
Kirstová M., Kundrata R. & Kočárek P. 2020. Molecular phylogeny and classification of Chelidurella Verhoeff, stat. restit. (Dermaptera: Forficulidae). Insect Systematics and Evolution 52 (3): 335–371. https://doi.org/10.1163/1876312X-bja10004
Kočárek P. 2004. Chelidura farkaci sp. n. (Dermaptera: Forficulidae) from China. Klapalekiana 40: 139–142.
Lapeira A. & Pascual F. 1980. Estudio preliminar de los dermápteros de la fauna ibérica. Trabajos Monográficos del Departamento de Zoología de la Universidad de Granada (n.s.) 3 (4) [1977]: 53–99.
Latreille P.A. 1825. Familles Naturelles du Règne Animal, Exposées Succintment et dans un Ordre Analytique avec l’indication de Leurs Genres. J.B. Baillière, Paris. https://doi.org/10.5962/bhl.title.16094
Linnaeus C. 1758. Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Volume I. L. Salvii, Stockholm. https://doi.org/10.5962/bhl.title.542
López Seoane V. 1885. On two forms of Rana from NW Spain. The Zoologist 9: 169–172.
Maccagno T. 1933. I Dermatteri Italiani. Bollettino dei Musei di Zoologia ed Anatomia Comparata della R. Università di Torino (ser. 3) 43 (40): 241–296.
Macher J.N., Rozenberg A., Pauls S.U., Tollrian R., Wagner R. & Leese F. 2015. Assessing the phylogeographic history of the montane caddisfly Thremma gallicum using mitochondrial and restriction site associated DNA (RAD) markers. Ecology and Evolution 5 (3): 648–662. https://doi.org/10.1002/ece3.1366
Martínez Freiría F., Velo Antón G. & Brito J.C. 2015. Trapped by climate: interglacial refuge and recent population expansion in the endemic Iberian adder Vipera seoanei. Diversity and Distributions 21 (3): 331–344. https://doi.org/10.1111/ddi.12265
Matzke D. & Kočárek P. 2015. Description and biology of Euborellia arcanum sp. nov., an alien earwig occupying greenhouses in Germany and Austria (Dermaptera: Anisolabididae). Zootaxa 3956: 131–139. https://doi.org/10.11646/zootaxa.3956.1.8
Mourier H. 1986. Notes on the life history of Labia minor (L.) (Dermaptera), a potential predator of housefly eggs and larvae (Diptera, Musca domestica L.). Entomologiske Meddelelser 53 (3): 143–148.
Neira Artidiello I. 2009. Nuevos datos de Pseudochelidura sinuata (La Fresnaye, 1825) para Asturias (España) (Dermaptera, Forficulidae). Boletín de la Sociedad Entomológica Aragonesa 44: 492.
Ollason J.G. 1970. Studies on Structural Variation in the Common European Earwig (Forficula auricularia Linn). PhD Thesis, Durham University. Available from http://etheses.dur.ac.uk/8617/ [accessed 11 Jan. 2023].
Oyston J.W., Hughes M., Wagner P.J., Gerber S. & Wills M.A. 2015. What limits the morphological disparity of clades? Interface Focus 5: 20150042. https://doi.org/10.1098/rsfs.2015.0042
Pérez Valcárcel J., López Colón J.I. & Prieto Piloña F. 2022. Aportaciones al inventario de los Dermaptera de la Península Ibérica. Arquivos Entomolóxicos 25: 351–366.
Pomorski R.J. 1990. Morphological-systematic studies on the variability of pseudocelli and some morphological characters in Onychiurus of the “armatus-group” (Collembola, Onychiuridae). Part II. On synonyms within the “armatus-group”, with special reference to diagnostic characters. Annales Zoologici 43: 535–576.
Pons J. 2006. DNA-based identification of preys from non-destructive, total DNA extractions of predators using arthropod universal primers. Molecular Ecology Notes 6: 623–626. https://doi.org/10.1111/j.1471-8286.2006.01353.x
Posada D. & Buckley T.R. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793–808. https://doi.org/10.1080/10635150490522304
Posso-Terranova A. & Andrés J. 2018. Multivariate species boundaries and conservation of harlequin poison frogs. Molecular Ecology 27: 3432–3451. https://doi.org/10.1111/mec.14803
QGIS Development Team. 2022. QGIS Geographic Information System. Open Source Geospatial Foundation Project. Versión 3.16. Available from https://qgis.org [accessed 11 Jan. 2023].
Rambaut A. 2012. FigTree, molecular evolution, phylogenetics and epidemiology. v.1.4. University of Edinburgh, Institute of Evolutionary Biology, Edinburgh. Available from http://tree.bio.ed.ac.uk/software/Figtree [accessed 11 Jan. 2023].
Rambur J. 1838. Faune entomologique de l’Andalusie Vol. II. Bertrand, Paris.
Recuero E. & García-París M. 2011. Evolutionary history of Lissotriton helveticus: multilocus assessment of ancestral vs. recent colonization of the Iberian Peninsula. Molecular Phylogenetics and Evolution 60: 170–182. https://doi.org/10.1016/j.ympev.2011.04.006
Rojo V., Giovannotti M., Naveira H., Nisi Cerioni P., González-Tizón A.M., Caputo Barucchi V., Galán P., Olmo E. & Martínez-Lage A. 2014. Karyological characterization of the endemic Iberian rock lizard, Iberolacerta monticola (Squamata, Lacertidae): insights into sex chromosome evolution. Cytogenetic and Genome Research 142: 28–39. https://doi.org/10.1159/000356049
Ronquist F., Teslenko M., Van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Ruiz J.L. & García-París M. 2015. Una nueva especie de Meloe Linnaeus, 1758 del grupo de M. (Eurymeloe) rugosus Marsham, 1802 (Coleoptera: Meloidae) del suroeste de Marruecos. Graellsia 71 (1): e018. https://doi.org/10.3989/graellsia.2015.v71.118
Sakai S. 1995. Dermapterorum Catalogus, XXVII: Iconographia XI. A basic Survey for Integrated Taxonomy of the Dermaptera of the World. Daito Bunka University, Tokyo.
Sánchez-Vialas A., García-París M., Ruiz J.L. & Recuero E. 2020. Patterns of morphological diversification in giant Berberomeloe blister beetles (Coleoptera: Meloidae) reveal an unexpected taxonomic diversity concordant with mtDNA phylogenetic structure. Zoological Journal of the Linnean Society 189 (4): 1249–1312. https://doi. org/10.1093/zoolinnean/zlz164
Schröder O., Cavanaugh K.K., Schneider J.V., Schell T., Bonada N., Seifert L. & Pauls S.U. 2021. Genetic data support local persistence in multiple glacial refugia in the montane net winged midge Liponeura cinerascens cinerascens (Diptera, Blephariceridae). Freshwater Biology 66 (5): 859–868. https://doi.org/10.1111/fwb.13682
Schwarz G. 1978. Estimating the dimension of a model. Annals of Statistics 6 (2): 461–464. https://doi.org/10.1214/aos/1176344136
Scudder S.H. 1876. Critical and historical notes on the Forficulariae; including description of new generic forms and an alphabetical synonymic list of the described species. Proceedings of the Boston Society of Natural History 18: 287–332. Available from https://www.biodiversitylibrary.org/page/41786331 [accessed 11 Jan. 2023].
Serville J.G.A. 1839. Histoire naturelle des Insects – Orthoptères. Librairie encyclopédique de Roret, Paris. https://doi.org/10.5962/bhl.title.16081
Simon C., Frati F., Beckenbach A., Crespi B., Liu H. & 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. https://doi.org/10.1093/aesa/87.6.651
Simpson G.B. & Mayer D.G. 1990. Morphometric analysis of variation in Nala lividipes (Dufour) and Labidura truncata Kirby (Dermaptera: Labiduridae). Australian Journal of Entomology 29 (4): 287–294. https://doi.org/10.1111/j.1440-6055.1990.tb00365.x
Sottile S., Cerasa G., Massa B. & Lo Verde G. 2022. Andricus cydoniae Giraud, 1859 junior synonym of Cynips conifica Hartig, 1843, as experimentally demonstrated (Hymenoptera: Cynipidae: Cynipini). Insects 13: 200. https://doi.org/10.3390/insects13020200
Srivastava G.K. 1970. Notes on a collection of Dermaptera from India (Dermaptera). Eos, Revista Española de Entomología 45 (1–4) [1969]: 319–333. Available from http://hdl.handle.net/10261/164269 [accessed 11 Jan. 2023].
Steinmann H. 1979. The Dermaptera in the PAN Zoologiczny Instytut, Warszawa. Folia Entomologica Hungarica 32: 149–175.
Steinmann H. 1981. The Dermaptera of the Universitetets Zoologiske Museum Kobenhavn. Folia Entomologica Hungarica 42: 173–192.
Steinmann H. 1993. Dermaptera: Eudermaptera II. Tierreich 108. Walter de Gruyter, Berlin, New York. https://doi.org/10.1515/9783110872705
Swofford D.L. 2002. PAUP*: Phylogenic Analysis Using Parsimony (* and other Methods). Sinauer, Sunderland.
Verhoeff K.W. 1902. Über Dermapteren. Versuch eines neuen, natürlicheren Systems auf vergleichend morphologischer Grundlage und über den Mikrothorax der Insecten. Zoologischer Anzeiger 25: 181–208.
Vigna Taglianti A. 1999. Notes on some Anechurinae from Appenines (Dermaptera, Forficulidae). Bollettino dell’Associazione Romana di Entomologia 54: 33–57.
Werren J.H., Baldo L. & Clark M.E. 2008. Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6 (10): 741–751. https://doi.org/10.1038/nrmicro1969
Wiley E.O. 1978. The evolutionary species concept reconsidered. Systematic Zoology 27: 17–26. https://doi.org/10.2307/2412809
Copyright (c) 2023 Amonio David Cuesta-Segura, Pilar Jurado-Angulo, Yolanda Jiménez-Ruiz, Mario García-París
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.
