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

Discordance between morphological species identification and mtDNA phylogeny in the flesh fly genus Ravinia (Diptera : Sarcophagidae)

Evan S. Wong A D , Gregory A. Dahlem B , Trevor I. Stamper C and Ronald W. DeBry A
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, 614 Rieveschl Hall, University of Cincinnati, Cincinnati, OH 45221, USA.

B Department of Biological Sciences, 248 Natural Sciences Building, Northern Kentucky University, Highland Heights, KY 41099, USA.

C Department of Entomology, 901 W. State Street, Purdue University, West Lafayette, IN 47907, USA.

D Corresponding author. Email: wonges@mail.uc.edu

Invertebrate Systematics 29(1) 1-11 https://doi.org/10.1071/IS14018
Submitted: 4 April 2014  Accepted: 16 September 2014   Published: 20 March 2015

Abstract

In order to better understand the phylogenetic relationships among species in the genus Ravinia Robineau-Desvoidy, 1863, we analysed data from two mitochondrial gene fragments: cytochrome oxidase I (COI) and cytochrome oxidase II (COII). We used Bayesian inference and maximum likelihood methods to infer phylogenetic relationships. Our results indicate that the genera Ravinia and Chaetoravinia, previously synonymised into the genus Ravinia (sensu lato) are each likely to be monophyletic (posterior probability 1; bootstrap support 85%). We found highly supported paraphyletic relationships among species of Ravinia, with relatively deep splits in the phylogeny. This conflict between the morphological species definitions and the mtDNA phylogeny could be indicative of the presence of cryptic species in Ravinia anxia (Walker, 1849), Ravinia floridensis (Aldrich, 1916), Ravinia lherminieri (Robineau-Desvoidy, 1830), and Ravinia querula (Walker, 1849).

Additional keywords: COI, COII, Chaetoravinia, mitochondrial DNA, molecular, morphology, phylogenetics, North America.


References

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In ‘Second International Symposium on Information Theory’. (Eds B. N. Petrov and F. Caski.) pp. 267–281. (Akademiai Kiado: Budapest, Hungary.)

Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |

Aldrich, J. M. (1916). Sarcophaga and allies in North America. Entomological Society of America. (Murphy-Divins Co. Press: Lafayette, IN, USA.)

Aldrich, J. M. (1930). Notes on the types of American two-winged flies of the genus Sarcophaga and a few related forms, described by the early authors. Proceedings of the United States National Museum 78, 1–39.

Bofkin, L., and Goldman, N. (2007). Variation in evolutionary processes at different codon positions. Molecular Biology and Evolution 24, 513–521.
Variation in evolutionary processes at different codon positions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhslyitr4%3D&md5=e7232b0ea20798722397e349bb87880fCAS | 17119011PubMed |

Caterino, M. S., Cho, S., and Sperling, F. A. H. (2000). The Current State of Insect Molecular Systematics: A Thriving Tower of Babel. Annual Review of Entomology 45, 1–54.
The Current State of Insect Molecular Systematics: A Thriving Tower of Babel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVequrg%3D&md5=8e3232e7a0fe7bb9d0ef957eba52a9d1CAS | 10761569PubMed |

Caletka, B. C., and McAllister, B. F. (2004). A genealogical view of chromosomal evolution and species delimitation in the Drosophila virilis species subgroup. Molecular Phylogenetics and Evolution 33, 664–670.
A genealogical view of chromosomal evolution and species delimitation in the Drosophila virilis species subgroup.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1Wjsb8%3D&md5=e40ce7dc23365907cfcf4889bf22acd5CAS | 15522794PubMed |

Clary, D. O., and Wolstenholme, D. R. (1985). The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution 22, 252–271.
The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xht1eqtb4%3D&md5=94b83b86bdb06ed4e6cd1ec648e440a7CAS | 3001325PubMed |

Dodge, H. R. (1956). New North American Sarcophagidae, with some new synonymy (Diptera). Annals of the Entomological Society of America 49, 182–190.

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=5e5a51a2851e50039acd3b34601cddcbCAS | 15034147PubMed |

Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.
Phylogenies and the comparative method.Crossref | GoogleScholarGoogle Scholar |

Geyer, C. J. (1991). Markov chain Monte Carlo maximum likelihood. In ‘Computing Science and Statistics: Proceedings of the 23rd Symposium on the Interface’. (Ed. E. M. Keramides.) pp.156–163. (Interface Foundation: Fairfax Station, USA.)

Gilks, W. R., and Roberts, G. O. (1996). Strategies for improving MCMC. In ‘Markov chain Monte Carlo in Practice’. (Eds W. R. Gilks, S. Richardson and D. J. Spiegelhalter.) pp. 89–114. (Chapman & Hall: London, UK.)

Giroux, M., Pape, T., and Wheeler, T. (2010). Towards a phylogeny of the flesh flies (Diptera: Sarcophagidae): Morphology and phylogenetic implications of the acrophallus in the subfamily Sarcophaginae. Zoological Journal of the Linnean Society 158, 740–778.
Towards a phylogeny of the flesh flies (Diptera: Sarcophagidae): Morphology and phylogenetic implications of the acrophallus in the subfamily Sarcophaginae.Crossref | GoogleScholarGoogle Scholar |

Guo, Y. D., Cai, J. F., Li, X., Xiong, F., Su, R. N., Chen, F. L., Liu, Q. L., Wang, X. H., Chang, Y. F., Zhong, M., Wang, X., and Wen, J. F. (2010). Identification of the forensically important sarcophagid flies Boerttcherisca peregrina, Parasarcophaga albiceps and Parasarcophaga dux (Diptera: Sarcophagidae) based on COII gene in China. Tropical Biomedicine 27, 451–460.
| 1:STN:280:DC%2BC3M3mt12kuw%3D%3D&md5=e84efdcfde6230b303bb449d03375f6cCAS | 21399586PubMed |

Hall, D. G. (1928). Sarcophaga pallinervis and related species in the Americas. Annals of the Entomological Society of America 21, 331–352.

Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004a). 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, 14 812–14 817.
Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVyju7g%3D&md5=779b1bd0f1967ad399e1391eed756639CAS |

Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., and Francis, C. M. (2004b). Identification of birds through DNA barcodes. PLoS Biology 2, e312.
Identification of birds through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Jordaens, K., Sonet, G., Richet, R., Dupont, E., Braet, Y., and Desmyter, S. (2013). Identification of forensically important Sarcophaga species (Diptera: Sarcophagidae) using the mitochondrial COI gene. International Journal of Legal Medicine 127, 491–504.
Identification of forensically important Sarcophaga species (Diptera: Sarcophagidae) using the mitochondrial COI gene.Crossref | GoogleScholarGoogle Scholar | 22960880PubMed |

Kutty, S. J., Pape, T., Wiegmann, B. M., and Meier, R. (2010). Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidae and the position of Mystacinobiidae and McAlpine’s fly. Systematic Entomology 35, 614–635.
Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidae and the position of Mystacinobiidae and McAlpine’s fly.Crossref | GoogleScholarGoogle Scholar |

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=69a56250f99303ede6ba715e4dc41f26CAS | 22319168PubMed |

Lim, G. S., Balke, M., and Meier, R. (2012). Determining species boundaries in a world full of rarity: singletons, species delimitation methods. Systematic Biology 61, 165–169.
Determining species boundaries in a world full of rarity: singletons, species delimitation methods.Crossref | GoogleScholarGoogle Scholar | 21482553PubMed |

Lopes, H. S. (1969). Family Sarcophagidae. In ‘A Catalogue of the Diptera of the Americas South of the United States, Vol. 103’. (Ed. N. Papavero.) pp. 1–88. (Departmento de Zoologia, Secretaria da Agricultura: São Paulo, Brazil.)

Lopes, H. S. (1982). The importance of the mandible and clypeal arch of the first instar larvae in the classification of the Sarcophagidae (Diptera). Revista Brasileira de Biologia 26, 293–326.

Maddison, W. P., and Maddison, D. R. (2011). ‘Mesquite 2.73: a modular system for evolutionary analysis.’ Available at http://mesquiteproject.org.

Meier, R., Shiyang, K., Vaidya, G., and Ng, P. K. L. (2006). DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology 55, 715–728.
DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success.Crossref | GoogleScholarGoogle Scholar | 17060194PubMed |

Meiklejohn, K. A., Wallman, J. F., and Dowton, M. (2011). DNA-based identification of forensically important Australian Sarcophagidae (Diptera). International Journal of Legal Medicine 125, 27–32.
DNA-based identification of forensically important Australian Sarcophagidae (Diptera).Crossref | GoogleScholarGoogle Scholar | 19997851PubMed |

Meiklejohn, K. A., Wallman, J. F., Cameron, S. L., and Dowton, M. (2012). Comprehensive evaluation of DNA barcoding for the molecular species identification of forensically important Australian Sarcophagidae (Diptera). Invertebrate Systematics 26, 515–525.
Comprehensive evaluation of DNA barcoding for the molecular species identification of forensically important Australian Sarcophagidae (Diptera).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKqtLvI&md5=9c6466ca82a435d3cbc5fac145320976CAS |

Meiklejohn, K. A., Wallman, J. F., and Dowton, M. (2013a). DNA Barcoding Identifies all Immature Life Stages of a Forensically Important Flesh Fly (Diptera: Sarcophagidae). Journal of Forensic Sciences 58, 184–187.
DNA Barcoding Identifies all Immature Life Stages of a Forensically Important Flesh Fly (Diptera: Sarcophagidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivFehsbg%3D&md5=aa38fc3f6463cb51d9a182964e33c808CAS | 23311518PubMed |

Meiklejohn, K. A., Wallman, J. F., Pape, T., Cameron, S. L., and Dowton, M. (2013b). Utility of COI, CAD and morphological data for resolving relationships within the genus Sarcophaga (sensu lato) (Diptera: Sarcophagidae): A preliminary study. Molecular Phylogenetics and Evolution 69, 133–141.
Utility of COI, CAD and morphological data for resolving relationships within the genus Sarcophaga (sensu lato) (Diptera: Sarcophagidae): A preliminary study.Crossref | GoogleScholarGoogle Scholar | 23665035PubMed |

Moore, W. S. (1995). Inferring phylogenies from mtDNA variation: Mitochondrial gene trees versus nuclear gene trees. Evolution 49, 718–726.
Inferring phylogenies from mtDNA variation: Mitochondrial gene trees versus nuclear gene trees.Crossref | GoogleScholarGoogle Scholar |

Pape, T. (1994). The world Blaesoxipha Loew, 1861 (Diptera: Sarcophagidae). Entomologica Scandinavica 45, 1–247.

Pape, T. (1996). Genus Ravinia Robineau-Desvoidy. In ‘Catalogue of the Sarcophagidae of the world (Insecta: Diptera)’. pp. 284–290. (Associated Publishers: Gainesville, FL, USA.)

Pape, T., and Dahlem, G. A. (2010). Sarcophagidae (flesh flies). In ‘Manual of Central American Diptera, Volume 2’. (Eds B. V. Brown et al.) pp. 1313–1335. (NRC Research Press: Ottawa, Ontario.)

Parker, R. R. (1914). Sarcophagidae of New England: males of the genera Ravinia and Boettcheria. Proceedings of the Boston Society of Natural History 35, 1–77.

Pickens, L. G. (1981). The life history and predatory efficiency of Ravinia lherminieri (Diptera: Sarcophagidae) on the face fly (Diptera: Muscidae). Canadian Entomologist 113, 523–526.
The life history and predatory efficiency of Ravinia lherminieri (Diptera: Sarcophagidae) on the face fly (Diptera: Muscidae).Crossref | GoogleScholarGoogle Scholar |

Rambaut, A., and Drummond, A. J. (2007). ‘Tracer (Version 1.4).’ Available at http://beast.bio.ed.ac.uk/TRACER.

Reid, N. M., and Carstens, B. C. (2012). Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology 12, 196–206.
Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model.Crossref | GoogleScholarGoogle Scholar | 23031350PubMed |

Robineau-Desvoidy, J. B. (1863). ‘Histoire naturelle des Dipteres des environs de Paris.’ Vol. 2. (Paris, France.)

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=6c22440a111ffd7c39b671a54462b45bCAS | 12912839PubMed |

Shapiro, B., Rambaut, A., and Drummond, A. J. (2006). Choosing appropriate substitution models for phylogenetic analysis of protein-coding sequences. Molecular Biology and Evolution 23, 7–9.
Choosing appropriate substitution models for phylogenetic analysis of protein-coding sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtleqtLvP&md5=0217689fd2e090730ef6a8d148320c2aCAS | 16177232PubMed |

Smith, M. A., Wood, D. A., Janzen, D. H., Hallwacks, W., and Hebert, P. D. N. (2007). DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences of the United States of America 104, 4967–4972.
DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFKiurw%3D&md5=39635e77dd53ab2b382d7e66f3418b8aCAS | 17360352PubMed |

Song, H., Buhay, J. E., Whiting, M. F., and Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105, 13486–13491.
Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChs7vP&md5=43b4a28cb788f88e7a9f80cb7b539dfaCAS | 18757756PubMed |

Sperling, F. A. H., Anderson, G. S., and Hickey, D. A. A. (1994). DNA-based approach to the identification of insect species used for post-mortem interval estimation. Journal of Forensic Sciences 39, 418–427.
| 1:CAS:528:DyaK2MXhtFCrsQ%3D%3D&md5=a9965f5017349bb3627b4e2c82652c15CAS |

Spillings, B. L., Brooke, B. D., Koekemoer, L. L., Chiphwanya, J., Coetzee, M., and Hunt, R. H. (2009). A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. The American Journal of Tropical Medicine and Hygiene 81, 510–515.
| 1:CAS:528:DC%2BD1MXhtFequrvM&md5=73d0227d81d4cfa4e23e7c562b24635eCAS | 19706923PubMed |

Stamper, T., Dahlem, G. A., Cookman, C., and DeBry, R. W. (2013). Phylogenetic relationships of flesh flies in the subfamily Sarcophaginae based on three mtDNA fragments (Diptera: Sarcophagidae). Systematic Entomology 38, 35–44.
Phylogenetic relationships of flesh flies in the subfamily Sarcophaginae based on three mtDNA fragments (Diptera: Sarcophagidae).Crossref | GoogleScholarGoogle Scholar |

Sukumaran, J., and Holder, M. T. (2010). DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571.
DendroPy: a Python library for phylogenetic computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVOltb0%3D&md5=1a2fa20c12ea16c78289c31c6305924dCAS | 20421198PubMed |

Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.
| 1:CAS:528:DyaK3sXks1CksL4%3D&md5=6a8e66bca4cdb41c232d8ea2cb89de5dCAS | 8336541PubMed |

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolution genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolution genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=421e650591d1feaa34697a0db6b94378CAS | 21546353PubMed |

Tan, S. H., Rizman-Idid, M., Mohd-Aris, E., Kurahashi, H., and Mohamed, Z. (2010). DNA-based characterization and classification of forensically important flesh flies (Diptera: Sarcophagidae) in Malaysia. Forensic Science International 199, 43–49.
DNA-based characterization and classification of forensically important flesh flies (Diptera: Sarcophagidae) in Malaysia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWrtbk%3D&md5=3fbe482f20e4ce1dad3bda10f21f2329CAS | 20392577PubMed |

Wells, J. D., and Stevens, J. R. (2009). Molecular methods for forensic entomology. In ‘Forensic Entomology: The Utility of Arthropods in Legal Investigations’, 2nd edn. (Eds J. H. Byrd and J. L. Castner.) pp. 439–455. (CRC Press: London, UK.)

Wiens, J. J., and Penkrot, T. L. (2002). Delimiting species based on DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology 51, 69–91.
Delimiting species based on DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus).Crossref | GoogleScholarGoogle Scholar | 11943093PubMed |

Wiens, J. J., and Servedio, M. R. (2000). Species delimitation in systematics: Inferring diangnostic difference between species. Proceedings. Biological Sciences 267, 631–636.
Species delimitation in systematics: Inferring diangnostic difference between species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czovFagtQ%3D%3D&md5=20095645ab617db2750e27135f6cf345CAS |

Zwikl, D. J. (2006). ‘Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion.’ Ph.D. thesis, The University of Texas: Austin, TX.