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Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Phylogeny of the African ball-rolling dung beetle genus Epirinus Reiche (Coleoptera : Scarabaeidae : Scarabaeinae)

S. Mlambo A B , C. L. Sole A and C. H. Scholtz A
+ Author Affiliations
- Author Affiliations

A Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa.

B Corresponding author. Email: smlambo@zoology.up.ac.za

Invertebrate Systematics 25(3) 197-207 https://doi.org/10.1071/IS10032
Submitted: 30 September 2010  Accepted: 30 May 2011   Published: 18 November 2011

Abstract

Recent phylogenetic analyses have pointed to the dung beetle genus Epirinus as the putative African ancestral roller group. Consequently, we tested the roller status of species in the genus with observational studies and constructed a molecular phylogeny based on partial sequences of two mitochondrial and two nuclear genes for 16 of 29 species. Tested species were confirmed to be dung rollers. Monophyly of the genus was confirmed, lending support to the synonymy of the wingless genus Endroedyantus with Epirinus. Moreover, the phylogenetic hypothesis was found to have a similar topology with a previously published one based on morphological data. A combined molecular and morphology analysis showed congruence between the molecular and morphological datasets. The loss of flight in some species and estimated divergence dates within Epirinus are discussed.


References

Baker, R. H., Yu, X., and DeSalle, R. (1998). Assessing the relative contribution of molecular and morphological characters in simultaneous analysis trees. Molecular Phylogenetics and Evolution 9, 427–436.
Assessing the relative contribution of molecular and morphological characters in simultaneous analysis trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVKkurk%3D&md5=bcabf701c30b9bc8b2c1dc074306eb90CAS |

Brower, A. V. Z. (1994). Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91, 6491–6495.
Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1KrsLw%3D&md5=6b2310e0d8437681aca1d49fc00a2f09CAS |

Brower, A. V. Z. (2006). The how and why of branch support and partitioned branch support, with a new index to assess partition incongruence. Cladistics 22, 378–386.
The how and why of branch support and partitioned branch support, with a new index to assess partition incongruence.Crossref | GoogleScholarGoogle Scholar |

Brown, J., Scholtz, C. H., Janeau, J.-L., Grellier, S., and Podwojewski, P. (2010). Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties. Applied Soil Ecology 46, 9–16.
Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties.Crossref | GoogleScholarGoogle Scholar |

Cambefort, Y. (1991). Biogeography and evolution. In ‘Dung Beetle Ecology’. (Eds I. Hanski and Y. Cambefort.) pp. 51–67. (Princeton University Press: Princeton, NJ.).

Davis, A. L. V., Scholtz, C. H., Dooley, P. W., Bham, N., and Kryger, U. (2004). Scarabaeine dung beetles as indicators of biodiversity, habitat transformation and pest control chemicals in agro-ecosystems. South African Journal of Science 100, 415–424.

Davis, A. L. V., Frolov, A. V., and Scholtz, C. H. (2008). ‘The African Dung Beetle Genera.’ (Protea Book House: Pretoria.)

Deschodt, C. M., and Scholtz, C. H. (2008). Systematics of South African forest-endemic dung beetles: new genera and species of small Canthonini (Scarabaeidae: Scarabaeinae). African Entomology 16, 91–106.
Systematics of South African forest-endemic dung beetles: new genera and species of small Canthonini (Scarabaeidae: Scarabaeinae).Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., and Rambaut, A. (2007). Beast: Bayesian Evolutionary Analysis Sampling Trees. BMC Evolutionary Biology 7, 214.
Beast: Bayesian Evolutionary Analysis Sampling Trees.Crossref | GoogleScholarGoogle Scholar |

Eeley, H. A. C., Lawes, M. J., and Piper, S. E. (1999). The influence of climate change on the distribution of indigenous forest in KwaZulu–Natal, South Africa. Journal of Biogeography 26, 595–617.
The influence of climate change on the distribution of indigenous forest in KwaZulu–Natal, South Africa.Crossref | GoogleScholarGoogle Scholar |

Fabre, J.-H. (1918). ‘The Sacred Beetle and Others.’ (Dodd, Mead and Company: New York.)

Farrell, B. D. (2001). Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. Molecular Phylogenetics and Evolution 18, 467–478.
Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1ansbc%3D&md5=e4ff6b1fd2a2a6835e2c8ac4ccc89057CAS |

Forgie, S. A., Philips, K., and Scholtz, C. H. (2005). Evolution of Scarabaeini (Scarabaeidae: Scarabaeinae). Systematic Entomology 30, 60–96.
Evolution of Scarabaeini (Scarabaeidae: Scarabaeinae).Crossref | GoogleScholarGoogle Scholar |

Forgie, S. A., Kryger, U., Bloomer, P., and Scholtz, C. H. (2006). Evolutionary relationships among the Scarabaeini (Coleoptera: Scarabaeidae) based on combined molecular and morphological data. Molecular Phylogenetics and Evolution 40, 662–678.
Evolutionary relationships among the Scarabaeini (Coleoptera: Scarabaeidae) based on combined molecular and morphological data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFWktLs%3D&md5=d02d2de4ed06c544f966858cb901787dCAS |

Gill, B. D. (1991). Dung beetles in tropical American forests. In ‘Dung Beetle Ecology’. (Eds I. Hanski and Y. Cambefort.) pp. 211–229. (Princeton University Press: Princeton, NJ.)

Gillespie, J. J., Munro, J. B., Heraty, J. M., Yoder, M. J., Owen, A. K., and Carmichael, A. E. (2005). A secondary structural of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution 22, 1593–1608.
A secondary structural of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFWhsb8%3D&md5=d734913009eb0c5f5b5c9bd4f404fe2dCAS |

Halffter, G., and Matthews, E. G. (1966). The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomologica Mexicana 12–14, 1–312.

Hanski, I., and Cambefort, Y. (1991). ‘Dung Beetle Ecology.’ (Princeton University Press: Princeton, NJ.)

Harrison, J. du G., and Philips, T. K. (2003). Phylogeny of Scarabaeus (Pachysoma MacLeay) stat. nov., and related flightless Scarabaeini (Scarabaeidae: Scarabaeinae). Annals of the Transvaal Museum 40, 47–71.

Holter, P., and Scholtz, C. H. (2005). Are ball-rolling (Scarabaeini, Gymnopleurini, Sisyphini) and tunneling scarabaeine dung beetles equally choosy about the size of ingested dung particles? Ecological Entomology 30, 700–705.
Are ball-rolling (Scarabaeini, Gymnopleurini, Sisyphini) and tunneling scarabaeine dung beetles equally choosy about the size of ingested dung particles?Crossref | GoogleScholarGoogle Scholar |

Juan, C., Oromi, P., and Hewitt, G. M. (1995). Phylogeny of the genus Hegeter (Tenebrionidae, Coleoptera) and its colonization of the Canary Islands deduced from cytochrome oxidase I mitochondrial DNA sequences. Proceedings of the Royal Society of London 261, 173–180.
Phylogeny of the genus Hegeter (Tenebrionidae, Coleoptera) and its colonization of the Canary Islands deduced from cytochrome oxidase I mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXoslKlu74%3D&md5=4ab347c1661f67a07810617a0fc743b0CAS |

Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286–298.
Recent developments in the MAFFT multiple sequence alignment program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1artrs%3D&md5=b175a27565b960e0440189ae5eb49d96CAS |

Korbie, D. J., and Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nature Protocols 3, 1452–1456.
Touchdown PCR for increased specificity and sensitivity in PCR amplification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOnsL7F&md5=37fbd7b19166fd2593a2770ee2d95609CAS |

Medina, C. A., and Scholtz, C. H. (2005). Systematics of the southern African genus Epirinus Reiche (Coleoptera: Scarabaeinae: Canthonini): descriptions of new species and phylogeny. Insect Systematics & Evolution 36, 145–160.
Systematics of the southern African genus Epirinus Reiche (Coleoptera: Scarabaeinae: Canthonini): descriptions of new species and phylogeny.Crossref | GoogleScholarGoogle Scholar |

Medina, C. A., Scholtz, C. H., and Gill, B. D. (2003). Morphological variation and systematics of Canthon Hoffmansegg 1817, and related genera in New World Canthonini dung beetles (Coleoptera, Scarabaeinae). Mitteilungen aus dem Museum für Naturkunde Berlin. Deutsche Entomologische Zeitschrift 50, 23–68.
Morphological variation and systematics of Canthon Hoffmansegg 1817, and related genera in New World Canthonini dung beetles (Coleoptera, Scarabaeinae).Crossref | GoogleScholarGoogle Scholar |

Monaghan, M. T., Inward, D. G., Hunt, T. H., and Vogler, A. P. (2007). A molecular phylogenetic analysis of the Scarabaeinae (dung beetles). Molecular Phylogenetics and Evolution 45, 674–692.
A molecular phylogenetic analysis of the Scarabaeinae (dung beetles).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKhsr7P&md5=c29df8cd02bef9d11f3fdcd910e89ceaCAS |

Moulton, J. K., and Wiegmann, B. M. (2004). Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged eremoneuran Diptera (Insecta). Molecular Phylogenetics and Evolution 31, 363–378.
Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged eremoneuran Diptera (Insecta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFSksbw%3D&md5=08d9652db0636774122ee880ed23f10cCAS |

Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S., Favila, M. E., and The Scarabaeinae Research Network (2008). Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141, 1461–1474.
Ecological functions and ecosystem services provided by Scarabaeinae dung beetles.Crossref | GoogleScholarGoogle Scholar |

Nylander, J. A. A. (2004). MrModeltest, version 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala. Available at http://www.abc.se/~nylander/ [verified September 2011]

Ocampo, F. C., and Hawks, D. C. (2006). Molecular phylogenetics and evolution of the food relocation behaviour of the dung beetle tribe Eucraniini (Coleoptera: Scarabaeidae: Scarabaeinae). Invertebrate Systematics 20, 557–570.
Molecular phylogenetics and evolution of the food relocation behaviour of the dung beetle tribe Eucraniini (Coleoptera: Scarabaeidae: Scarabaeinae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVKrtb%2FE&md5=58f794e788f2d480fe9f05ec894f992aCAS |

Orsini, L., Koivulehto, H., and Hanski, I. (2007). Molecular evolution and radiation of dung beetles in Madagascar. Cladistics 23, 145–168.
Molecular evolution and radiation of dung beetles in Madagascar.Crossref | GoogleScholarGoogle Scholar |

Philips, K. T., Pretorius, E., and Scholtz, C. H. (2004). A Phylogenetic analysis of dung beetles (Scarabaeinae: Scarabaeidae): unrolling an evolutionary history. Invertebrate Systematics 18, 53–88.
A Phylogenetic analysis of dung beetles (Scarabaeinae: Scarabaeidae): unrolling an evolutionary history.Crossref | GoogleScholarGoogle Scholar |

Rahagalala, P., Viljanen, H., Hottola, J., and Hanski, I. (2009). Assemblages of dung beetles using cattle dung in Madagascar. African Entomology 17, 71–89.
Assemblages of dung beetles using cattle dung in Madagascar.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=2e3026ffe4fe8a7047647a21d09682feCAS |

Rutschmann, F. (2006). Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times. Diversity & Distributions 12, 35–48.
Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times.Crossref | GoogleScholarGoogle Scholar |

Scholtz, C. H. (2000). Evolution of flghtlessness in Scarabaeoidea (Insecta, Coleoptera). Mitteilungen aus dem Museum für Naturkunde Berlin. Deutsche Entomologische Zeitschrift 47, 5–28.

Scholtz, C. H., and Howden, H. F. (1987). A revision of the southern African genus Epirus Reiche (Coleoptera: Scarabaeidae: Scarabaeinae). Journal of the Entomological Society of southern Africa 50, 121–154.

Scholtz, C. H., Davis, A. L. V., and Kryger, U. (2009). ‘Evolutionary Biology and Conservation of Dung Beetles.’ (Pensoft Publishers: Sofia, Bulgaria.)

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and 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.
| 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=e18cd8adc97253298926722223656b77CAS |

Smith, C. I., and Farrell, B. D. (2005). Range expansions in the flightless longhorn cactus beetles, Moneilema armatum, in response to Pleistocene climate changes. Molecular Ecology 14, 1025–1044.
Range expansions in the flightless longhorn cactus beetles, Moneilema armatum, in response to Pleistocene climate changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFalt78%3D&md5=599da47d368f1ff8b12b26d6a74fe209CAS |

Sole, C. L., and Scholtz, C. H. (2010). Did dung beetles arise in Africa? A phylogenetic hypothesis based on five gene regions. Molecular Phylogenetics and Evolution 56, 631–641.
Did dung beetles arise in Africa? A phylogenetic hypothesis based on five gene regions.Crossref | GoogleScholarGoogle Scholar |

Sole, C. L., Scholtz, C. H., and Bastos, A. D. S. (2005). Phylogeography of the Namib Desert dung beetles Scarabaeus (Pachysoma) MacLeay (Coleoptera: Scarabaeidae). Journal of Biogeography 32, 75–84.
Phylogeography of the Namib Desert dung beetles Scarabaeus (Pachysoma) MacLeay (Coleoptera: Scarabaeidae).Crossref | GoogleScholarGoogle Scholar |

Sorenson, M. D., and Franzosa, E. A. (2007). TreeRot, version 3. Boston University, Boston, MA. Available at http://people.bu.edu/msoren/TreeRot.html [verified September 2011]

Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis Using Parsimony (and other methods), version 4. (Sinauer Associates: Sunderland, MA.) Available at http://paup.csit.fsu.edu/downl.html [verified September 2011]

Vogler, A. P., DeSalle, R., Assmann, T., Knisley, C. B., and Schultz, T. D. (1993). Molecular population genetics of the endangered tiger beetle, Cicindela dorsalis (Coleoptera: Cicindelidae). Annals of the Entomological Society of America 86, 142–152.

Wahlberg, N., and Wheat, C. W. (2008). Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Systematic Biology 57, 231–242.
Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVymsr%2FL&md5=3c7159f311b16c19d7227a2a9e2495c6CAS |

Wild, A. L., and Maddison, D. R. (2008). Evaluating nuclear protein-coding genes for phylogenetic utility in beetles. Molecular Phylogenetics and Evolution 48, 877–891.
Evaluating nuclear protein-coding genes for phylogenetic utility in beetles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyntL3M&md5=e1dc8d4d2d8c4f7d300c025e6d794521CAS |

Winterton, S. L., Hardy, N. B., and Wiegman, B. M. (2010). On wings of lace: phylogeny and Bayesian divergence time estimates of Neuropterida (Insecta) based on morphological and molecular data. Systematic Entomology 35, 349–378.
On wings of lace: phylogeny and Bayesian divergence time estimates of Neuropterida (Insecta) based on morphological and molecular data.Crossref | GoogleScholarGoogle Scholar |

Wirta, H., and Montreuil, O. (2008). Evolution of the Canthonini Longitarsi (Scarabaeidae) in Madagascar. Zoologica Scripta 37, 651–663.
Evolution of the Canthonini Longitarsi (Scarabaeidae) in Madagascar.Crossref | GoogleScholarGoogle Scholar |

Wirta, H., Orsini, L., and Hanski, I. (2008). An old adaptive radiation of forest dung beetles in Madagascar. Molecular Phylogenetics and Evolution 47, 1076–1089.
An old adaptive radiation of forest dung beetles in Madagascar.Crossref | GoogleScholarGoogle Scholar |