Eur. J. Entomol. 116: 52-63, 2019 | DOI: 10.14411/eje.2019.006

First DNA analysis of pill scarabs (Coleoptera: Hybosoridae: Ceratocanthinae) reveals multiple paraphyly of Afrotropical PhilharmostesOriginal article

Vasily V. GREBENNIKOV
Canadian Food Inspection Agency, 960 Carling Ave., Ottawa, ON, K1A 0Y9, Canada; e-mail: vasily.grebennikov@canada.ca

This paper is the first attempt to resolve relationships among the Ceratocanthinae: Ceratocanthini pill scarab beetles using DNA sequences. It is focused on the Philharmostes group of seven Afrotropical genera: Baloghianestes (3 spp.), Callophilharmostes (1 sp.), Carinophilharmostes (1 sp.), Chaetophilharmostes (1 sp.), Cryptophilharmostes (3 spp.), Petrovitzostes (1 sp.) and Philharmostes (31 spp.). A phylogenetic analysis of 46 terminals and alignment of 2,913 bp from one mitochondrial and two nuclear fragments corroborates monophyly of this group, but rejects that of Philharmostes, the largest genus. The latter is paraphyletic with respect to at least four other smaller genera and consists of at least three distantly related clades. One of them, formed by Philharmostes ballerioi sp. n. from the Tanzanian Nguru (the type locality) and Kaguru Mountains, is sister to the rest of the entire Philharmostes group. The nominal genus Philharmostes is, therefore, a waste-basket taxon for accommodating members of this group that lack the distinct characters of the smaller genera. Pending further research, the phylogenetically inadequate generic taxonomy of the Philharmostes group is not modified. Molecular clock analysis estimates separation of the mitochondrial lineages of two known populations of the new species at about 2.2 Ma, which corresponds with recurring shrinkage and expansion of African rainforest caused by climatic fluctuations during the Pleistocene. Adults of all nominal ingroup genera are illustrated along with male and female body parts of the new species. Diagnostic and/or synapomorphic morphological characters of the Philharmostes group of genera are revised. Habitus images and other supplementary information on all sequenced specimens are available online at dx.doi.org/10.5883/DS-VGDS001 and dx.doi.org/10.5883/DS-VGDS004.

Keywords: Coleoptera, Hybosoridae, Ceratocanthinae, Ceratocanthini, DNA barcode, ITS2, 28S, phylogeny, forest litter, taxonomy, Philharmostes ballerioi sp. n., Afrotropical Region, Eastern Arc Mountains

Received: September 6, 2018; Revised: November 5, 2018; Accepted: November 5, 2018; Published online: February 19, 2019  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
GREBENNIKOV, V.V. (2019). First DNA analysis of pill scarabs (Coleoptera: Hybosoridae: Ceratocanthinae) reveals multiple paraphyly of Afrotropical Philharmostes. EJE116, Article 52-63. https://doi.org/10.14411/eje.2019.006
Download citation

References

  1. Andújar C., Serrano J. & Gómez-Zurita J. 2012: Winding up the molecular clock in the genus Carabus (Coleoptera: Carabidae): assessment of methodological decisions on rate and node age estimation. - BMC Evol. Biol. 12: 40, 16 pp. Go to original source...
  2. Ballerio A. 2000: A new genus and species of Ceratocanthidae from Tanzania (Coleoptera: Scarabaeoidea). - Afr. Zool. 35: 131-137. Go to original source...
  3. Ballerio A. 2001: Description of Philharmostes werneri n. sp. from Tanzania with notes on the "Philharmostes" generic group (Coleoptera, Ceratocanthidae). - Fragm. Entomol. 33: 147-157.
  4. Ballerio A. 2016: A first phylogenetic appraisal of two allied genera of Afrotropical Ceratocanthinae: Melanophilharmostes and Pseudopterorthochaetes (Coleoptera: Hybosoridae). - Fragm. Entomol. 48: 33-52. Go to original source...
  5. Ballerio A. & Grebennikov V.V. 2016: Rolling into a ball: phylogeny of the Ceratocanthinae (Coleoptera: Hybosoridae) inferred from adult morphology and origin of a unique body enrollment coaptation in terrestrial arthropods. - Arthr. Syst. Phylog. 74: 23-52. Go to original source...
  6. Ballerio A., Gill B.D. & Grebennikov V.V. 2011: Illustrated overview and identification key to Cameroonian Ceratocanthinae beetles (Coleoptera: Scarabaeoidea: Hybosoridae) with description of four new species. - Zootaxa 2892: 1-24. Go to original source...
  7. Beutel R.G., Yea E., Richter A., Büsse S., Miller K.B., Yavorskaya M. & Wipfler B. 2017: The head of Heterogyrus milloti (Coleoptera: Gyrinidae) and its phylogenetic implications. - Arthr. Syst. Phylog. 75: 261-280. Go to original source...
  8. Cantino P.D. & de Queiroz K. 2014: International Code of Phylogenetic Nomenclature. Ver. 5. URL: https://www.ohio.edu/phylocode/
  9. Choate P.M. 1987: Biology of Ceratocanthus aenius (Coleoptera: Scarabaeidae: Ceratocanthinae). - Fla Entomol. 70: 301-305. Go to original source...
  10. de Queiroz K. & Gauthier J. 1990: Phylogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. - Syst. Zool. 39: 307-322. Go to original source...
  11. de Queiroz K. & Gauthier J. 1992: Phylogenetic taxonomy. - Annu. Rev. Ecol. Syst. 23: 449-480. Go to original source...
  12. D'Hotman D. & Scholtz C.H. 1990: Phylogenetic significance of the structure of the external male genitalia in the Scarabaeoidea (Coleoptera). - Entomol. Mem. Dep. Agric. Dev. Rep. Sth Afr. 77: 1-51.
  13. Drummond A.J., Suchard M.A., Xie D. & Rambaut A. 2012: Bayesian phylogenetics with BEAUti and the BEAST 1.7. - Mol. Biol. Evol. 29: 1969-1973. Go to original source...
  14. Fairmaire L. 1899: Matériaux pour la faune coléoptérique de la région Malgache. 9e note. - Ann. Soc. Entomol. Fr. 68: 466-507.
  15. Felsenstein J. 1985: Confidence limits on phylogenies: an approach using the bootstrap. - Evolution 39: 783-791. Go to original source...
  16. Fjeldså J. & Lovett J.C. 1997: Geographical patterns of old and young species in African forest biota: the significance of specific montane areas as evolutionary centres. - Biodiv. Conserv. 6: 325-346. Go to original source...
  17. Grebennikov V.V. 2008: A featherwing beetle without wings: re-discovery and second species of Rioneta (Coleoptera: Ptiliidae) from the Uluguru Mountains, Tanzania. - Zootaxa 1732: 45-53. Go to original source...
  18. Grebennikov V.V. 2017: Phylogeography and sister group of Lupangus, a new genus for three new flightless allopatric forest litter weevils endemic to the Eastern Arc Mountains, Tanzania (Coleoptera: Curculionidae, Molytinae). - Fragm. Entomol. 49: 37-55. Go to original source...
  19. Grebennikov V.V. 2018: Dryophthorinae weevils (Coleoptera: Curculionidae) of the forest floor in Southeast Asia: Three-marker analysis reveals monophyly of Asian Stromboscerini and new identity of rediscovered Tasactes. - Eur. J. Entomol. 115: 437-444. Go to original source...
  20. Grebennikov V.V. & Heiss E. 2018: Survey and DNA barcoding of flat bugs (Hemiptera: Aradidae) in the Tanzanian Forest Archipelago reveal a phylogeographically structured fauna largely unknown at the species level. - Eur. J. Entomol. 115: 512-523. Go to original source...
  21. Grebennikov V.V. & Scholtz C.H. 2004: The basal phylogeny of Scarabaeoidea (Insecta: Coleoptera) inferred from larval morphology. - Invertebr. Syst. 18: 321-348. Go to original source...
  22. Grebennikov V.V., Ballerio A., Ocampo F. & Scholtz C.H. 2004: Larvae of Ceratocanthidae and Hybosoridae (Coleoptera: Scarabaeoidea): study of morphology, phylogenetic analysis and evidence of paraphyly of Hybosoridae. - Syst. Entomol. 29: 524-543. Go to original source...
  23. Hamilton A.C. & Taylor D. 1991: History of climate and forests in tropical Africa during the last 8 million years. - Climat. Change 19: 65-78. Go to original source...
  24. Heads M. 2014: Biogeography of Australasia: A Molecular Analysis. Cambridge University Press, Cambridge, 503 pp. Go to original source...
  25. Hebert P.D.N., Cywinska A., Ball S.L. & DeWaard J.R. 2003a: Biological identifications through DNA barcodes. - Proc. R. Soc. (B) 270: 313-321. Go to original source...
  26. Hebert P.D.N., Ratnasingham S. & DeWaard J.R. 2003b: Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. - Proc. R. Soc. (B) 270: 96-99. Go to original source...
  27. Howden H.F. & Gill B.D. 2000: Tribes of New World Ceratocanthinae, with keys to genera and descriptions of new species (Coleoptera: Scarabaeidae). - Sociobiology 35: 281-329.
  28. Katoh K. & Toh H. 2008a: Recent developments in the MAFFT multiple sequence alignment program. - Brief. Bioinform. 9: 286-298. Go to original source...
  29. Katoh K. & Toh H. 2008b: Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. - BMC Bioinform. 9: 212, 13 pp. Go to original source...
  30. Katoh K., Misawa K., Kuma K. & Miyata T. 2002: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. - Nucl. Acids Res. 30: 3059-3066. Go to original source...
  31. Kirk-Spriggs A.H. & Muller B.S. 2017: Biogeography of Diptera. In Kirk-Spriggs A.H. & Sinclair B.J. (eds): Manual of Afrotropical Diptera. Vol. 1. Introductory Chapters and Key to Diptera Families. Suricata 4. South African National Biodiversity Institute, Pretoria, pp. 203-238.
  32. Kolbe H.J. 1895: Beiträge zur Kenntnis der Mistkäfer, Lamellicornia onthophila. - Stett. Entomol. Ztg 56: 329-345.
  33. Krell F.T. & Cranston P.S. 2004: Which side of the tree is more basal? - Syst. Entomol. 29: 279-281. Go to original source...
  34. Kumar S., Stecher G. & Tamura K. 2016: MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. - Mol. Biol. Evol. 33: 1870-1874. Go to original source...
  35. Lovett J.C. & Wasser S.K. (eds) 1993: Biogeography and Ecology of the Rain Forests of Eastern Africa. Cambridge University Press, Cambridge, 351 pp. Go to original source...
  36. Maddison W.P. & Maddison D.R. 2011: Mesquite: a modular system for evolutionary analysis. Version 3.11. Program and documentation. URL: http://mesquiteproject.org (last accessed 15 Nov. 2017).
  37. Miller M., Pfeiffer W. & Schwartz T. 2010: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA. IEEE, New Orleans, pp. 1-8. Go to original source...
  38. Ocampo F.C. & Hawks D.C. 2006: Phylogenetic analysis of the scarab family Hybosoridae and monographic revision of the New World subfamily Anaidinae (Coleoptera: Scarabaeoidea). 2. Molecular phylogenetics and systematic placement of the family Hybosoridae (Coleoptera: Scarabaeoidea). - Bull. Univ. Nebraska State Mus. 19: 7-12.
  39. Omland K.E., Cook L.G. & Crisp M.D. 2008: Tree thinking for all biology: the problem with reading phylogenies as ladders of progress. - BioEssays 30: 854-867. Go to original source...
  40. Papadopoulou A., Anastasiou I. & Vogler A.P. 2010: Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. - Mol. Biol. Evol. 27: 1659-1672. Go to original source...
  41. Parker J. 2016: Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. - Myrmecol. News 22: 65-108.
  42. Paulian R. 1968: The scientific results of the Hungarian soil zoological expedition to the Brazzaville - Congo. 33. Espèces de la famille Acanthoceridae (Coleoptera: Scarabaeoidea). - Opusc. Zool. (Budapest) 8: 87-98.
  43. Paulian R. 1977: Révision des Ceratocanthidae (Coleoptera, Scarabaeidae). I. Les formes africaines. - Rev. Zool. Afr. 91: 253-316.
  44. Poe S., Nieto-Montes de Oca A., Torres-Carvajal O., de Queiroz K., Velasco J.V., Truett B., Gray L.N., Ryan M.J., Köhler G., Ayala-Varela F. & Latella I. 2017: A phylogenetic, biogeographic, and taxonomic study of all extant species of Anolis (Squamata; Iguanidae). - Syst. Biol. 66: 663-697. Go to original source...
  45. Ratnasingham S. & Hebert P.D.N. 2007: BOLD: the barcode of life data system. - Mol. Ecol. Notes 7: 355-364. Go to original source...
  46. Stamatakis A. 2006: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. - Bioinformatics 22: 2688-2690. Go to original source...
  47. Stamatakis A., Hoover P. & Rougemont J. 2008: A rapid bootstrap algorithm for the RAxML web servers. - Syst. Biol. 57: 758-771. 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.