Organisms Diversity & Evolution

, Volume 17, Issue 1, pp 181–198 | Cite as

Revised classification and phylogeny of an Afrotropical species group based on molecular and morphological data, with the description of a new genus (Coleoptera: Scarabaeidae: Onthophagini)

  • Angela Roggero
  • Enrico Barbero
  • Claudia Palestrini
Original Article

Abstract

The worldwide distributed Onthophagus genus comprises at present more than 2000 species, that often show a complicated and uncertain systematic history. In particular, the many Afrotropical species included in this genus have never been entirely reviewed after the division into 32 species groups proposed by d’Orbigny in 1913, although subsequent researches focusing on some of these species suggested that Onthophagus constituted a nonmonophyletic taxon. In order to highlight their phylogenetic relationships, the various Afrotropical species groups of d’Orbigny must thus be examined, and it would be advisable to study them separately to avoid misunderstanding. In this framework, the taxonomic position of the three species currently included in the 21st d’Orbigny group was examined. Both morphological and biomolecular analyses contributed in confirming that these species (i.e., Onthophagus caffrarius d’Orbigny, 1902; Onthophagus quadraticeps Harold, 1867; and Onthophagus signatus Fåhraeus, 1857) constituted a well-defined monophyletic group that cannot be maintained within the genus Onthophagus. Therefore, the Kurtops gen.n. is here described to accommodate these Afrotropical species, that are nevertheless always included within the Onthophagini tribe. On the basis of the phylogenetic relationships here elucidated, it was also emphasized that the new genus is strictly related to Digitonthophagus and Phalops; thus, it was proposed to include the three genera into a single clade of suprageneric rank naming it as Phalops complex.

Keywords

Onthophagus New genus Phalops complex Molecular analysis Morphological analysis Phylogeny Geometric morphometrics 

Notes

Acknowledgments

The research was partly funded by the Italian Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR). The iconographic material was produced using the facilities of the Laboratory of Geometric Morphometrics at the Department of Life Sciences and Systems Biology of Torino, equipped thanks to the funds from the CRT Foundation, Research and Education section (Torino, Italy). We are grateful to museum curators and private collectors for the loan of the material. We want also to thank J. Willers (ZMHB, Berlin, Germany) and M. Balke (ZSM, Munich, Germany) for useful information about the type material. We are greatly indebted to the two anonymous reviewers who contributed to improving our manuscript with many useful suggestions. We thank also our colleague Dan Chamberlain that made a thorough revision of the English text.

Supplementary material

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References

  1. Ahrens, D., Schwarzer, J., & Vogler, A. P. (2014). The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proceedings of the Royal Society B, 281, 2014–1470. doi: 10.1098/rspb.2014.1470.CrossRefGoogle Scholar
  2. Balthasar, V. (1959). Beitrag zur Kenntnis der Gattung Onthophagus. Acta Entomologica Musei Nationalis Pragae, 33, 461–471.Google Scholar
  3. Balthasar, V. (1963). Monographie der Scarabaeidae und Aphodiidae der palaearktischen und orientalischen Region. Coleoptera: Lamellicornia. Vol. 2. Prag: Verlag der Tschechoslowakischen Akademie der Wissenschaften.Google Scholar
  4. Barbero, E., Palestrini, C., & Roggero, A. (2003). Revision of the genus Phalops Erichson, 1848 (Coleoptera: Scarabaeidae: Onthophagini). Torino: Museo Regionale di Scienze Naturali.Google Scholar
  5. Bryant, D., & Moulton, V. (2004). NeighborNet: an agglomerative algorithm for the construction of phylogenetic networks. Molecular Biology and Evolution, 21, 255–265.CrossRefPubMedGoogle Scholar
  6. Casiraghi, M., Labra, M., Ferri, E., Galimberti, A., & De Mattia, F. (2010). DNA barcoding: a six-question tour to improve users’ awareness about the method. Briefing in Bioinformatics, 11, 440–453. doi: 10.1093/bib/bbq003.CrossRefGoogle Scholar
  7. Chevasco, V., Elzinga, J. A., Mappes, J., & Grapputo, A. (2014). Evaluation of criteria for species delimitation of bagworm moths (Lepidoptera: Psychidae). European Journal of Entomology, 111, 121–136. doi: 10.14411/eje.2014.013.CrossRefGoogle Scholar
  8. d’Orbigny, H. (1913). Synopsis des Onthophagides d’Afrique. Annales de la Société Entomologique de France, 82, 1–742.Google Scholar
  9. Del Latte, L., Bortolin, F., Rota-Stabelli, O., Fusco, G., & Bonato, L. (2015). Molecular-based estimate of species number, phylogenetic relationships and divergence times for the genus Stenotaenia (Chilopoda, Geophilomorpha) in the Italian region. ZooKeys, 510, 31–47. doi: 10.3897/zookeys.510.8808.CrossRefGoogle Scholar
  10. Dincă, V., Wiklund, C., Lukhtanov, V. A., Kodandaramaiah, U., Norén, K., Dapporto, L., Wahlberg, N., Vila, R., & Friberg, M. (2013). Reproductive isolation and patterns of genetic differentiation in a cryptic butterfly species complex. Journal of Evolutionary Biology, 26, 2095–2106. doi: 10.1111/jeb.12211.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dincă, V., Montagud, S., Talavera, G., Hernández-Roldán, J., Munguira, M. L., García-Barros, E., Hebert, P. D. H., & Vila, R. (2015). DNA barcode reference library for Iberian butterflies enables a continental-scale preview of potential cryptic diversity. Scientific Reports, 5, 12395. doi: 10.1038/srep12395.CrossRefPubMedPubMedCentralGoogle Scholar
  12. d’Orbigny, H. (1902). Mémoire sur les Onthophagides d’Afrique. Annales de la Société entomologique de France, 71, 1–324.Google Scholar
  13. Eberhard, W. G. (1992). Species isolation, genital mechanics, and the evolution of species-specific genitalia in three species of Macrodactylus beetles (Coleoptera, Scarabeidae, Melolonthinae). Evolution, 46, 1774–1783.CrossRefGoogle Scholar
  14. Emlen, D. J. I., Marangelo, J., Ball, B., & Cunningham, C. W. (2005). Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution, 59, 1060–1084.CrossRefPubMedGoogle Scholar
  15. Fåhraeus, O. L. (1857). Insecta Caffraria annis 1838–1845 a J.A.Wahlberg collecta amici auxilios sultus descripsit. Coleoptera. Holmiae, 2, 1–395.Google Scholar
  16. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.CrossRefGoogle Scholar
  17. Gilligan, T. M., & Wenzel, J. W. (2008). Extreme intraspecific variation in Hystrichophora (Lepidoptera: Tortricidae) genitalia—questioning the lock-and-key hypothesis. Annales Zoologici Fennici, 45, 465–477.CrossRefGoogle Scholar
  18. Goloboff, P.A., Farris, J.S. & Nixon K.C. (2003) TNT: tree analysis using new technology. [Free software available through the Hennig Society] URL http://www.zmuc.dk/public/phylogeny/TNT/. Accessed 15 Jan 2016.
  19. Goloboff, P. A., Farris, J. S., & Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.CrossRefGoogle Scholar
  20. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.CrossRefPubMedGoogle Scholar
  21. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.CrossRefPubMedGoogle Scholar
  22. Hebert, P. D. N., Cywinska, A., Ball, S. L., & Dewaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B, 270, 313–322.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., & Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101, 14812–14817.CrossRefPubMedPubMedCentralGoogle Scholar
  24. House, C. M., & Simmons, L. W. (2003). Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proceedings of the Royal Society of London - Series B, 270, 447–455. doi: 10.1098/rspb.2002.2266.CrossRefPubMedPubMedCentralGoogle Scholar
  25. House, C. M., & Simmons, L. W. (2005). Relative influence of male and female genitalia morphology on paternity in the dung beetle Onthophagus taurus. Behavioral Ecology, 16, 889–897.CrossRefGoogle Scholar
  26. Huelsenbeck, J. P., Ronquist, F., Nielsen, R., & Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.CrossRefPubMedGoogle Scholar
  27. Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.CrossRefPubMedGoogle Scholar
  28. IBM Corp. (2013). IBM SPSS statistics for Windows, version 22.0. Released. Armonk: IBM Corp.Google Scholar
  29. King, R. A., Read, D. S., Traugott, M., & Symondson, W. O. C. (2008). Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology, 17, 947–963. doi: 10.1111/j.1365-294X.2007.03613.x.CrossRefPubMedGoogle Scholar
  30. Masly, J. P. (2012). 170 years of “lock-and-key”: genital morphology and reproductive isolation. International Journal of Evolutionary Biology, 2012, 247352. doi: 10.1155/2012/247352. 10 pages.CrossRefPubMedGoogle Scholar
  31. Medina, C., Molano, F., & Scholtz, C. H. (2013). Morphology and terminology of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) male genitalia. Zootaxa, 3626, 455–476.CrossRefPubMedGoogle Scholar
  32. Mikkola, K. (2008). The lock-and-key mechanisms of the internal genitalia of the Noctuidae (Lepidoptera): how are they selected for? European Journal of Entomology, 105, 13–25. doi: 10.14411/eje.2008.002.CrossRefGoogle Scholar
  33. Mlambo, S., Sole, C. L., & Scholtz, C. H. (2015). A molecular phylogeny of the African Scarabaeinae (Coleoptera: Scarabaeidae). Arthropod Systematics & Phylogeny, 73, 303–321.Google Scholar
  34. Monaghan, M. T., Inward, D. G., Hunt, T., & Vogler, A. P. (2007). A molecular phylogenetic analysis of the Scarabaeinae (dung beetles). Molecular Phylogenetics and Evolution, 45, 674–692. doi: 10.1016/j.ympev.2007.06.009.CrossRefPubMedGoogle Scholar
  35. Moretto, P. (2009). Essai de classification des Onthophagus Latreille, 1802 africains des 5ème et 6ème groupes de d’Orbigny (Coleoptera, Scarabaeidae). Nouvelle Revue d’Entomologie, 25, 145–178.Google Scholar
  36. Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.Google Scholar
  37. Pizzo, A., Roggero, A., Palestrini, C., Cervella, P., Del Pero, M., & Rolando, A. (2006). Genetic and morphological differentiation patterns between sister species: the case of Onthophagus taurus and Onthophagus illyricus (Coleoptera, Scarabaeidae). Biological Journal of the Linnean Society, 89, 197–211.CrossRefGoogle Scholar
  38. Pizzo, A., Roggero, A., Palestrini, C., Moczek, A., & Rolando, A. (2008). Rapid shape divergences between natural and introduced populations of a horned beetle partly mirror divergences between species. Evolution & Development, 10, 166–175.CrossRefGoogle Scholar
  39. Rambaut, A. (2014). FigTree v1.4.2. url http://tree.bio.ed.ac.uk/software/. Accessed 15 Jan 2016.
  40. Rambaut, A., Suchard, M. & Drummond, A.J. (2013). Tracer v1.6. URL http://tree.bio.ed.ac.uk/software/. Accessed 15 Jan 2016.
  41. Ratnasingham, S., & Hebert, P. D. N. (2007). BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes, 7, 355–364. doi: 10.1111/j.1471-8286.2006.01678.x.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ratnasingham, S., & Hebert, P. D. N. (2013). A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE, 8, e66213. doi: 10.1371/journal.pone.0066213.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Roggero, A., Giachino, P. M., & Palestrini, C. (2013). A new cryptic ground beetle species from the Alps characterised via geometric morphometrics. Contributions to Zoology, 82, 171–183.Google Scholar
  44. Roggero, A., Barbero, E., & Palestrini, C. (2015). Phylogenetic and biogeographical review of the Drepanocerina (Coleoptera: Scarabaeidae: Oniticellini). Arthropod Systematics and Phylogeny, 73, 153–174.Google Scholar
  45. Rohlf, F.J. (2015). tpsDig v2.20. url http://life.bio.sunysb.edu/morph/morph.html/. Accessed 15 Jan 2016.
  46. Rohlf, F.J. (2015). tpsUtil v1.64. url http://life.bio.sunysb.edu/morph/morph.html/. Accessed 15 Jan 2016.
  47. Rohlf, F.J. (2015) tpsSmall v1.33. url http://life.bio.sunysb.edu/morph/morph.html/. Accessed 15 Jan 2016.
  48. Rohlf, F.J. (2015). tpsRelw v1.54. url http://life.bio.sunysb.edu/morph/morph.html. Accessed 15 Jan 2016.
  49. Rohlf, F.J. (2015). tpsRegr v1.42. url http://life.bio.sunysb.edu/morph/morph.html. Accessed 15 Jan 2016.
  50. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  51. Ronquist, F., Huelsenbeck, J.P. & Teslenko, M. (2011). MrBayes v3.2. url http://mrbayes.net/. Accessed 15 Jan 2016.
  52. Sharkey, M. J., Carpenter, J. M., Vilhelmsen, L., Heraty, J., Liljeblad, J., Dowling, A. P. G., Schulmeister, S., Murray, D., Deans, A. R., Ronquist, F., Krogmann, L., & Wheeler, W. C. (2012). Phylogenetic relationships among superfamilies of Hymenoptera. Cladistics, 28, 80–112. doi: 10.1111/j.1096-0031.2011.00366.x.CrossRefGoogle Scholar
  53. Simmons, M. (2014). A confounding effect of missing data on character conflict in maximum likelihood and Bayesian MCMC phylogenetic analyses. Molecular Phylogenetics and Evolution, 80, 267–280.CrossRefPubMedGoogle Scholar
  54. Simmons, L. W., & Garcia-Gonzales, F. (2011). Experimental coevolution of male and female genital morphology. Nature Communications, 2, 374. doi: 10.1038/ncomms1379.CrossRefPubMedGoogle Scholar
  55. Swofford, D. L. (2002). PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4b.10. Sunderland: Sinauer Associates.Google Scholar
  56. Tagliaferri, F., Moretto, P., & Tarasov, S. I. (2012). Essai sur la systématique et la phylogénie des Onthophagus Latreille, 1802, d’Afrique tropicale appartenant au septième groupe de d’Orbigny. Description d’un sous-genre nouveau et de trois espèces nouvelles (Coleoptera, Scarabaeoidea, Onthophagini). Catharsius La Revue, 6, 1–31.Google Scholar
  57. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Tarasov, S. I., & Génier, F. (2015). Innovative Bayesian and parsimony phylogeny of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae) enhanced by ontology-based partitioning of morphological characters. PlosOne, 10, e0116671. doi: 10.1371/journal.pone.0116671.CrossRefGoogle Scholar
  59. Tarasov, S. I., & Kabakov, O. N. (2010). Two new species of Onthophagus (Coleoptera: Scarabaeidae) from Indochina, with a discussion of some problems with the classification of Serrophorus and similar subgenera. Zootaxa, 2344, 17–28.Google Scholar
  60. Tarasov, S. I., & Solodovnikov, A. Y. (2011). Phylogenetic analyses reveal reliable morphological markers to classify mega-diversity in Onthophagini dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Cladistics, 27, 1–39.CrossRefGoogle Scholar
  61. Tocco, C., Roggero, A., Rolando, A., & Palestrini, C. (2011). Inter-specific shape divergence in Aphodiini dung beetles: the case of Amidorus obscurus and A. immaturus. Organisms, Diversity and Evolution, 11, 263–273.CrossRefGoogle Scholar
  62. Vodă, R., Dapporto, L., Dincă, V., & Vila, R. (2015). Why do cryptic species tend not to co-occur? A case study on two cryptic pairs of butterflies. PLoS ONE, 10, e0117802. doi: 10.1371/journal.pone.0117802.CrossRefPubMedPubMedCentralGoogle Scholar
  63. von Harold, E. (1867). Beiträge zur Kenntniss der Gattung Onthophagus. Coleopterologische Hefte, 2, 23–59.Google Scholar
  64. Wirta, H., Orsini, L., & Hanski, I. (2008). An old adaptive radiation of forest dung beetles in Madagascar. Molecular Phylogenetics and Evolution, 47, 1076–1089. doi: 10.1016/j.ympev.2008.03.010.CrossRefPubMedGoogle Scholar
  65. Wojcieszek, J. M., & Simmons, L. W. (2013). Divergence in genital morphology may contribute to mechanical reproductive isolation in a millipede. Ecology and Evolution, 3, 334–343.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zunino, M. (1981). Insects of Saudi Arabia. Coleoptera, Fam. Scarabaeidae, Tribus Onthophagini. Fauna of Saudi Arabia, 3, 408–416.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  1. 1.Department of Life Sciences and Systems BiologyUniversity of TurinTurinItaly

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