Abstract
The opatrine darkling beetles (Coleoptera: Tenebrionidae: Opatrini) are a worldwide radiation of ~1200 described species, with many more still awaiting discovery. This paper presents results of the first comparative morphological study of the female terminalia of this group. The structure of ovipositor and female genital tubes proved to be extremely useful for delimiting phylogenetic relationships within Opatrini. The following new lineages are recovered: Opatrum (basal parts of paraprocts equipped with claws constituted of baculi) and Sclerum (middle part of coxites soft and extended, apical lobe small and located laterally) generic complexes. Moreover, the analysis revealed that Heterotarsini and Heterocheirini share a unique vagina modification (presence of dual sclerites). Based on this observation, Heterocheirini is placed as a synonym of Heterotarsini. An additional comparative analysis of chosen external characters was performed to test hypotheses mentioned above. This investigation not only supports the conclusions derived from the female reproductive system analysis (Opatrum and Sclerum generic complexes; homogeneity of Heterotarsini and Heterocheirini), but also leads to the recovery of other presumably monophyletic groups (e.g., Blapsitnus generic complex). Finally, to test the explicitness of the current autapomorphy and determine the status of the whole studied group, a comparative morphological analysis of protrochanters among different tribes of Tenebrioninae was performed. All opatrine genera exhibit a unique protrochanter structure, which is characterized by the elongate base. This feature is unique for Opatrini among Tenebrioninae. Based on the above-mentioned results, the subtribal classification of the Opatrini is revised. Seven following subtribes are recognized: Ammobiina stat. restit., Blapstinina stat. restit., Heterotarsina (=Heterocheirini syn. nov.), Neopachypterina, Opatrina, Sclerina stat. restit. and Stizopina. Additionally, Wolladrus nom. nov. is proposed as a replacement name for Hadrus (Opatrini), which is a junior homonym of a dipteran genus.
Similar content being viewed by others
Notes
This name is proposed here as replacement name for Hadrus Wollaston, 1854 (Tenebrionidae: Opatrini), junior homonym of Hadrus Perty, 1833 (Insecta: Diptera). We dedicate this name to Thomas Vernon Wollaston (9th March 1822–4th January 1878), the author of the taxonomic conception of this genus.
References
Aalbu RL, Triplehorn CA (1985) Redefinition of the opatrine tribes in North America with notes on some apterous genera (Coleoptera: Tenebrionidae: Tenebrioninae). Coleopt Bull 39:272–280
Antoine M (1941) Notes d’entomologie marocaine. XXII. Les Litoborinae du Maroc (Col. Teneb.). Bulletin de la Société des Sciences Naturelles du Maroc 21:19–52
Antoine M (1956) Notes d’entomologie marocaine. LXIII. Sur la systématique des Litoborini et révision des Melambiina marocains. Bull Soc Sci Nat Phys Maroc 36:341–366
Banaszkiewicz M (2006) Comparative study of female genitalia in Pedinini (sensu Iwan 2004) (Coleoptera: Tenebrionidae: Pedinini), with notes on the classification. Ann Zool 56:59–77
Blaisdell FE (1909) A monographic revision of the Coleoptera belonging to the tenebrionide tribe Eleodiini inhabiting the United States, Lower California, and adjacent islands. Bulletin of the United States National Museum 63:1–524
Blanchard E (1845) Histoire des Insectes, traitant de leur moeurs et de leur métamorphoses en générale et comprenant une nouvelle classification fondée sur leur rapports naturelles. In: Traité Complet d’Histoire Naturelle. Histoires des Insectes. Tome II. Paris: Firmin Didot Frères, 524 pp
Bouchard P, Yeates DK (2001) Phylogenetic relationships of the Australasian Coelometopini (Coleoptera: Tenebrionidae); a quantitative cladistic analysis with a review of biology. Org Divers Evol 1:17–43
Bouchard P, Lawrence JF, Davies A, Newton AF (2005) Synoptic classification of the world Tenebrionidae (Insecta: Coleoptera) with a review of family-group names. Ann Zool 55:499–530
Bouchard P, Löbl I, Merkl O (2007) Nomenclatural notes on tenebrionid beeltes of the Palaeractic region (Insecta, Coleoptera). Annales Zoologici 57:385–394
Bouchard P, Bousquet Y, Davies AE, Alonso-Zarazaga MA, Lawrence JF, Lyal CHC, Newton AF, Reid CAM, Schmitt M, Ślipiński SA, Smith ABT (2011) Family-group names in Coleoptera (Insecta). ZooKeys 88:1–972
Brullé GA (1832) In: Bory de Saint-Vincent JBGM (ed) Expédition scientifique de Morée. Section des sciences physiques. Tome III.—1.re partie. Zoologie. Deuxième section.—Des animaux articulés. F.G. Levrault, Paris, [1] + 400 + [2 (errata)], pp 1–240
Desbrochers des Loges J (1902) Faunule des coléoptères de la France et de la Corse: Tenebrionidae (Suite). Le Frelon 11:1–56
Doyen JT (1972) Familial and subfamilial classification of the Tenebrionoidea (Coleoptera) and revised generic classification of the Coniontini. Quaest Entomol 8:357–376
Doyen JT, Tschinkel WR (1982) Phenetic and cladistic relationships among tenebrionid beetles (Coleoptera). Syst Entomol 7:127–183
Eschscholtz JF (1829) Zoologischer Atlas enthaltend Abbildungen neuer Thierarten, während des Flottcapitains von Kotzebue zweiter Reise um die Welt 1823–1826 gesammelt. Reimer, Berlin
Español F (1945) Nuevos comentarios sistemáticos sobre la subfamilia Opatrinae Reitt. con la descripción de un nuevo represenante del Sáhara Español (Col. Tenebrionidae). Eos Rev Esp Entomol 20:213–232
Ferrer J (2000) Contributions to the knowledge of the genera Scleropatrum Reitter, 1890 and Polycoelogastridium Reichardt, 1936 (Coleoptera, Tenebrionidae, Opatrini). Entomofauna 21:33–47
Ferrer J (2002) Révision de la sous-tribu Emmalina sensu Koch 1956. Les espèces du genre Emmalus Erichson (1843) nomen validum (=Emmallus Gebien, 1938) (Coleoptera, Tenebrionidae, Opatrini. Entomol Afr 7:23–63
Gebien H (1938) Katalog der Tenebrioniden. Teil II. Mitteilungen der Münchener Entomologische Gesellschaft 28: 49–80, 283–428 [370–465]
Geiselhardt SF, Geiselhardt S, Peschke K (2006) Chemical mimicry of cuticular hydrocarbons—how does Eremostibes opacus gain access to breeding burrows of its host Parastizopus armaticeps (Coleoptera, Tenebrionidae)? Chemoecology 16:59–68
ICZN (1999) International code of zoological nomenclature, 4th edn. International Trust for Zoological Nomenclature, London
Iwan D (2000) Ovoviviparity in tenebrionid beetles of the melanocratoid Platynotina (Coleoptera: Tenebrionidae: Platynotini) from Madagascar with notes on the viviparous beetles. Ann Zool 50:15–25
Iwan D (2001) Comparative study of male genitalia in Opatrinae sensu Medvedev (1968) (Coleoptera: Tenebrionidae), with notes on the tribal classification. Part I. Ann Zool 51:351–390
Iwan D (2002) Generic classification of the tribe Platynotini (Coleoptera: Tenebrionidae), with notes on phylogeny. Ann Zool 52:1–149
Iwan D (2004) A comparative study of male genitalia in Opatrinae sensu Medvedev (1968) (Coleoptera: Tenebrionidae), with notes on the reinterpreted tribal classification. Part II. Ann Zool 54:735–765
Iwan D (2008) Revision of the genus Reichardtiellina Kaszab, 1982 (Coleoptera: Opatrini). Ann Zool 58:731–744
Iwan D, Matthews EG (2015) Scleropatroides Löbl and Merkl (Coleoptera: Tenebrionidae: Opatrini) discovered in Australia, with description of a new species and discussion of related genera. Coleopt Bull 69(mo4):115–121
Iwan D, Schimrosczyk D (2009) Catalogue of the World Stizopina (Coleoptera: Tenebrionidae: Opatrini). Ann Zool 59:259–280
Iwan D, Schimrosczyk D (2015) Revision of the stizopoid genus Crististibes Koch, 1963 (Coleoptera: Tenebrionidae: Opatrini). Ann Zool 65:551–566
Iwan D, Ferrer J, Raś M (2010) Catalogue of the world Gonocephalum Solier, 1834 (Coleoptera, Tenebrionidae, Opatrini). Part 1. List of the species and subspecies. Ann Zool 60:245–304
Iwan D, Merkl O, Ferrer J (2011) Catalogue of the world Gonocephalum Solier, 1834 (Coleoptera: Tenebrionidae: Opatrini). Part 2. Comments, additions and references. Ann Zool 61:259–276
Kamiński MJ (2012) Taxonomy of the Afrotropical genera Angolositus Koch, 1955 and Pseudoselinus Iwan, 2002 with a key to species (Coleoptera: Tenebrionidae: Pedinini). Zootaxa 3500:49–60
Kamiński MJ (2015a) Notes on species diversity patterns in Stizopina (Coleoptera: Tenebrionidae), with description of a new genus from Nama Karoo. Ann Zool 65:131–148
Kamiński MJ (2015b) Phylogenetic reassessment and biogeography of the Ectateus generic group (Coleoptera: Tenebrionidae: Platynotina). Zool J Linn Soc 175:73–106
Kamiński MJ (2015c) Afrotropical Melambiina: four new species of Zadenos (Tenebrionidae: Pedinini), with notes on related taxa. Ann Zool 65:531–550
Kergoat GJ, Soldati L, Clamens AL, Jourdan H, Jabbour-Zahab R, Genson G, Bouchard P, Condamine FL (2014) Higher level molecular phylogeny of darkling beetles (Coleoptera: Tenebrionidae). Syst Entomol 39:486–499. doi:10.1111/syen.12065/pdf
Kirejtshuk AG, Merkl O, Kernegger F (2008) A new species of the genus Pentaphyllus Dejean, 1821 (Coleoptera, Tenebrionidae, Diaperinae) from the Baltic amber and checklist of the fossil Tenebrionidae. Zoosyst Ross 17:131–137
Kirejtshuk AG, Nabozhenko MV, Nel A (2010) New genus and species of the tribe Opatrini (Coleoptera, Tenebrionidae, Tenebrioninae) from the Lowermost Eocene amber of Paris Basin. Proc Zool Inst RAS 314:191–196
Koch C (1953) The Tenebrionidae of Southern Africa XXIV. In: Vorläufige Beschreibung neuer Tenebrionidaen des Südlichen Africas aus der Sammlung der Universität Lund, vol 49. Lund University Årsskrift N.F, pp 1–24
Koch C (1955) The Tenebrionidae of southern Africa XXV. New, forgotten or Palaearctic genera and species of Opatrinae. Ann Transvaal Mus 22:419–476
Koch C (1956) Exploration du Parc National de l’Upemba. II. Tenebrionidae (Coleoptera, Polyphaga), Opatrinae, first part: Platynotini, Litoborini and Loensini. Institut des Parcs nationaux du Congo Belge, Bruxelles
Koch C (1963) The Tenebrionidae of Southern Africa, 29. Luebbertia plana gen. & spec. nov. with a dichotomic analysis of Stizopina (Opatrini). Sci Pap Namib Desert Res Stn 18:1–87
Lacordaire T (1859) Histoire naturelle des Insectes. Generades Coléoptères ou exposé méthodique et critique de tousles genres proposés jusqu’ici dans ce ordre d’Insectes. Tome Cinquième. Librairie Encyclopédeique deRoret. Première partie, Paris, pp 1–400
Lawrence JF, Ślipiński A, Seago AE, Thayer MK, Newton AF, Marvaldi AE (2011) Phylogeny of the Coleoptera based on morphological characters of adults and larvae. Ann Zool 61:1–217
LeConte JL (1862) Classification of the Coleoptera of North America. Part I (cont.). Smithson Misc Collect 3:209–278
Marcuzzi G (1987) Description of the external female genitalia of some Neotropical Tenebrionidae (Coleoptera: Heteromera). Acta Zool Acad Sci Hung 33:87–112
Marcuzzi G (1989) Structure of genitalia and phylogenesis of Neotropical tenebrionids (Insecta: Coleoptera: Tenebrionidae). Senckenb Biol 69:345–367
Matthews EG, Bouchard P (2008) Tenebrionid Beetles of Australia: Descriptions of tribes, keys to genera, catalogue of species. Australian Biological Resources Study, Canberra, p viii + 398
Matthews EG, Merkl O (2015) Hangaya enigmatica, a new genus and species of Tenebrionidae from Central Australia (Coleoptera). Annales Zoologici 65:479–482
Matthews EG, Lawrence JF, Bouchard P, Steiner WE, Ślipiński SA (2010) 11.14 Tenebrionidae Latreille, 1802. In: Leschen RAB, Beutel RG, Lawrence JF (eds) Handbook of zoology. A natural history of the phyla of the animal kingdom. Vol. IV—Arthropoda: Insecta. Part 38. Coleoptera, Beetles. Vol 2: systematics. Walter de Gruyter, Berlin, pp 574–659
Medvedev GS (1968) Coleoptera. Darkling-beetles (Tenebrionidae), subfamily Opatrinae, tribes Platynotini, Dendarini, Pedinini, Dissonomini, Pachypterini, Opatrini (part) and Heterotarsini. Fauna of USSR, Leningrad
Mulsant E (1854) Histoire naturelle des coléoptères de France. Latigènes. L. Maison, Paris
Mulsant E, Rey C (1853) Suplément à la monographie des coléoptères trimères sécuripalpes. Annales de la Société Linnéenne de Lyon (Nouvelle Série) 1:129–333
Mulsant E, Rey C (1854) Essai d’une division des derniers Mélasomes. Mémoires de l’Académie Impériale des Sciences, Belles-Lettres et Arts de Lyon. Classe des Sciences. (Nouvelle série) 4:155–332
Penrith ML (1984) Two new species of Stizopina (Coleoptera: Tenebrionidae: Opatrini) from Namaqualand, southern Africa, and the relationships between the psammophilous genera. Ann Transvaal Mus 33:353–363
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rasa OAE (1994) Parabiosis and its proximate mechanisms in four Kalahari desert tenebrionid beetles. Ethology 98:137–148
Rasa OAE (1996) Interspecific association in desert tenebrionid beetles: a cleptoparasite does not affect the host’s reproductive success, but that of its offspring. Naturwissenschaften 83:575–577
Rasa OAE, Endrödy-Younga S (1997) Intergeneric associations of stizopinid tenebrionids relative to their geographical distribution (Coleoptera: Tenebrionidae: Opatrini: Stizopina). Afr Entomol 5:231–239
Reichardt AN (1936) Revision des Opatrines (Coleoptera Tenebrionidae) de la Région Paléarctique Tableaux Analytiques de la Faune de L’URSS. Institut Zoologique de l’Academie des Sciences, Moscou-Leningrad
Schawaller W (2013) The genus Heterotarsus Latreille (Coleoptera: Tenebrionidae: Opatrini) in South Africa and Namibia. Ann Ditsong Natl Mus Nat Hist 3:85–89
Seidlitz GC (1894) Tenebrionidae. In: Kiesenwetter GC (ed) Naturgeschichte der Insecten Deutschlands. Gebonnen von Dr. W. F. Erichson, fotgesetzt von Prof. Dr. H. Schaum, Dr. G. Kraatz, H. v. Kiesenwetter, Julius Weise, Edm. Reitter und DR. G. Seidlitz. Erste Abteilung Coleoptera. Fünfter Band. Erste Hälfe. Nicolaiche Verlags-Buchhandlung, Berlin
Skopin NG (1964) Die Larven der Tenebrioniden des Tribus Pycnocerini (Coleoptera Heteromera). Annales du Musée Royal de l’Afrique Centrale 127:1–35
Smith AD (2013) Phylogenetic revision of the North American Asidini (Coleoptera: Tenebrionidae). Syst Entomol 38:585–614
Tschinkel WR (1978) Ovoviviparity in some tenebrionid beetles. Coleopt Bull 32:315–317
Tschinkel WR, Doyen JT (1980) Comparative anatomy of the defensive glands, ovipositors and female genital tubes of tenebrionid beetles (Coleoptera). Int J Insect Morphol Embryol 9:321–368
Watt J (1974) A revised subfamily classification of Tenebrionidae (Coleoptera). N Z J Zool 11:381–452
Wickham H (2010) ggplot2: elegant graphics for data analysis. J Stat Softw 35:1–3
Acknowledgments
This research was founded by the SONATA 7 Project (Number 2014/13/D/NZ8/02428) from the National Science Centre, Poland. For valuable comments on the manuscript, the authors thank Aaron D. Smith (Northern Arizona University) and the anonymous reviewers assigned by the Editor.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Iwan, D., Kamiński, M.J. Toward a natural classification of opatrine darkling beetles: comparative study of female terminalia. Zoomorphology 135, 453–485 (2016). https://doi.org/10.1007/s00435-016-0328-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-016-0328-5