Molecular phylogenetics of the Muscidae (Diptera : Calyptratae): new ideas in a congruence context
Guilherme Schnell e Schuehli A C , Claudio José Barros de Carvalho A and Brian M. Wiegmann BA Departamento de Zoologia, Universidade Federal do Paraná, CP 19020, Curitiba 81.531-980, Brazil.
B North Carolina State University, Department of Entomology, College of Agriculture and Life Sciences, Gardner Hall, Campus Box 7613, Raleigh, NC 27695-7613, USA.
C Corresponding author. Email: schnell@onda.com.br
Invertebrate Systematics 21(3) 263-278 https://doi.org/10.1071/IS06026
Submitted: 12 July 2006 Accepted: 20 March 2007 Published: 27 June 2007
Abstract
Hypotheses about the evolution of Muscidae have long been the subject of continuous re-evaluation and reinterpretation. Current understandings of the relationships among these flies are based mainly on a single set of characters and are therefore questionable. Our understanding of muscid phylogeny thus needs greater support and further corroboration from additional suites of characters. In the current study, we analysed phylogenetic relationships among 24 species of muscid flies (18 genera and six subfamilies) using 2989 characters derived from sequences of mitochondrial (COI and COII) and nuclear genes (CAD and EF-1α). Data from each gene partition were analysed both in combined and separate phylogenetic analyses using maximum parsimony, maximum likelihood, and Bayesian inference. Support was found for the monophyly of the Muscidae in all analyses and for a sister-group relationship between Coenosiini and Phaoniinae. The latter group was placed in a clade with sampled species of Reinwardtiini and Cyrtoneurininae. The genera Ophyra and Hydrotaea were placed in the Muscinae and a sister-group relationship for Musca and Stomoxys was supported. Sampled species of Polietina form a monophyletic lineage, while Morellia was found to be paraphyletic. Combined analysis of gene partitions improved support and resolution for resulting topologies despite significant incongruence between data partitions found through application of the Incongruence Length Difference test.
Additional keywords: cytochrome oxidase, CAD, EF-1α, molecular systematics, Muscoidea, nuclear genes.
Acknowledgements
We gratefully acknowledge Walter Boeger, Marcia Souto Couri, Ana Maria Azeredo-Espin, Gabriel A. R. Melo and especially Marcio R. Pie for discussing the manuscript and their valuable suggestions. We also would like to express our thanks to Adrian Charles Pont, who provided the European species, and Lisete M. Lorini for the loan of several of the South American specimens included in the study. We appreciate the relevant comments made by the anonymous reviewers regarding this publication.
This project was supported by a fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (Programa de Doutorado com Estágio no Exterior – PDEE/BEX0143/02–2), and grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), process number 140700/2001–3 (GSS) and 304.148/2002–4 (CJBC), and the US National Science Foundation (0098745, BMW and J. Thorne; and 0334948, BMW). This paper is the contribution number 01707 of the Departamento de Zoologia da Universidade Federal do Paraná (DZUP).
Adams M. D.,
Celniker S. E.,
Holt R. A.,
Evans C. A., Gocayne J. D. , et al..
(2000) The genome sequence of Drosophila melanogaster. Science 287, 2185–2195.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Akaike H.
(1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
| Crossref | GoogleScholarGoogle Scholar |
Baker R. H., DeSalle R.
(1997) Multiple sources of character information and the phylogeny of the Hawaiian drosophilids. Systematic Biology 46, 654–673.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Baker R. H.,
Wilkinson G. S., DeSalle R.
(2001) Phylogenetic utility of different types of molecular data used to infer evolutionary relationships among Stalk-Eyed flies (Diopsidae). Systematic Biology 50, 87–105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beckenbach A. T., Borkent A.
(2003) Molecular analysis of the biting midges (Diptera: Ceratopogonidae), based on mitochondrial cytocrome oxidase subunit 2. Molecular Phylogenetics and Evolution 27, 21–35.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beckenbach A. T.,
Wei Y. W., Liu H.
(1993) Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences. Molecular Biology and Evolution 10, 619–634.
| PubMed |
Bernasconi M. V.,
Pawlowski J.,
Valsangiacomo C.,
Piffaretti J.-C., Ward P. I.
(2000a) Phylogeny of the Scathophagidae (Diptera, Calyptratae) based on mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 16, 308–315.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bernasconi M. V.,
Valsangiacomo C.,
Piffaretti J.-C., Ward P. I.
(2000b) Phylogenetic relationships among Muscoidea (Diptera: Calyptratae) based on mitochondrial DNA sequences. Insect Molecular Biology 9, 67–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bernasconi M. V.,
Pawlowski J.,
Valsangiacomo C.,
Piffaretti J.-C., Ward P. I.
(2001) Phylogeny of the genus Scathophaga (Diptera: Scathophagidae) inferred from mitochondrial DNA sequences. Canadian Journal of Zoology 79, 517–524.
| Crossref | GoogleScholarGoogle Scholar |
Bremer K.
(1988) The Limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42, 795–803.
| Crossref | GoogleScholarGoogle Scholar |
Bremer K.
(1994) Branch support and tree stability. Cladistics 10, 295–304.
| Crossref | GoogleScholarGoogle Scholar |
Brower A.
(1996) Combining data in phylogenetic analysis. Trends in Ecology & Evolution 11, 334–335.
| Crossref | GoogleScholarGoogle Scholar |
Brower A. V. Z., DeSalle R.
(1994) Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Annals of the Entomological Society of America 87, 702–716.
Brown J. M.,
Pellmyr O.,
Thompson J. N., Harrison R. G.
(1994) Phylogeny of Greya (Lepidoptera: Proxidae) based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Molecular Biology and Evolution 11, 128–141.
| PubMed |
Bull J. J.,
Huelsenbeck J. P.,
Cunningham C. W.,
Swofford D. L., Waddell P. J.
(1993) Partitioning and combining data in phylogenetic analysis. Systematic Biology 42, 384–397.
| Crossref | GoogleScholarGoogle Scholar |
Capaldi R. A.,
Malatesta F., Darley-Usmar V. M.
(1983) Structure of cytochrome oxidase. Biochimica et Biophysica Acta 726, 135–148.
| PubMed |
Carvalho C. J. B. de
(1989) Classificação de Muscidae (Diptera): uma proposta através da análise cladística. Revista Brasileira de Zoologia 6, 627–648.
Carvalho C. J. B. de
(1999) Revision, cladistics and biogeography of the neotropical genus Souzalopesmyia Albuquerque (Diptera: Muscidae). Proceedings of the Entomological Society of Washington 101, 123–137.
Carvalho C. J. B. de, Couri M. S.
(2002) A cladistic and biogeographic analysis of Apsil Malloch and Reynoldsia Malloch (Diptera, Muscidae) of southern South America. Proceedings of the Entomological Society of Washington 104, 309–317.
Carvalho C. J. B. de, Nihei S. S.
(2002) A new genus of Phaoniinae (Diptera: Muscidae) from Central America. Annales Zoologici 52, 327–331.
Carvalho C. J. B. de, Pont A. C.
(2006) Taxonomy, cladistics and biogeography of the South American genus Brachygasterina Macquart (Diptera: Muscidae). Zootaxa 1151, 1–26.
Carvalho C. J. B. de,
Pont A. C.,
Couri M. S., Pamplona D.
(2003) A catalogue of the Fannidae (Diptera) of the Neotropical Region. Zootaxa 210, 1–32.
Carvalho C. J. B. de,
Couri M. S.,
Pont A. C.,
Pamplona D., Lopes S. M.
(2005) A Catalogue of the Muscidae (Diptera) of the Neotropical Region. Zootaxa 860, 1–282.
Caterino M. S., Sperling F. A. H.
(1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Molecular Phylogenetics and Evolution 11, 122–137.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cho S.,
Mitchell A.,
Regier J. C.,
Mitter C.,
Poole C.,
Friedlander T. P., Zhao S.
(1995) A highly conserved nuclear gene for low-level phylogenetics: elongation factor 1-alpha recovers morphology-based tree for Heliothine moths. Molecular Biology and Evolution 12, 650–656.
| PubMed |
Collins K. P., Wiegmann B. M.
(2002) Phylogenetic relationships of the lower Cyclorrhapha (Diptera: Brachycera) based on 28s rDNA sequences. Insect Systematics and Evolution 33, 445–456.
Couri M. S., Carvalho C. J. B.
(1997) Revision of Polietina Schnabl & Dziedzicki (Diptera, Muscidae) and considerations on its new systematic position. Revista. Revista Brasileira de Zoologia 14, 255–281.
Couri M. S., Carvalho C. J. B. de
(2003) Systematic relations among Philornis Meinert, Passeromyia Rodhain & Villeneuve and allied genera (Diptera, Muscidae). Brazilian Journal of Biology 63, 223–232.
| Crossref | GoogleScholarGoogle Scholar |
Couri M. S., Pont A. C.
(2000) A cladistic analysis of Coenosiinae (Diptera, Muscidae). Systematic Entomology 25, 373–392.
| Crossref | GoogleScholarGoogle Scholar |
Cunningham C. W.,
Zhu H., Hillis D. M.
(1998) Best-fit maximum-likelihood models for phylogenetic inference: empirical tests with known phylogenies. Evolution 52, 978–987.
| Crossref | GoogleScholarGoogle Scholar |
Cuny R.
(1980) Revision of the genus Eudasyphora Townsend (Diptera: Muscidae), and reflections on its evolution. Canadian Entomologist 112, 345–373.
Danforth B. N., Ji S.
(1998) Elongation factor-1α occurs as two copies in bees: implications for phylogenetics analysis of EF-1α in insects. Molecular Biology and Evolution 15, 225–235.
| PubMed |
Eastwood R., Hughes J. M.
(2003) Molecular phylogeny and evolutionary biology of Acrodipsas (Lepidoptera: Lycaenidae). Molecular Phylogenetics and Evolution 27, 93–102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Farris J. S.,
Källersjö M.,
Kluge A. G., Bult C.
(1994) Testing significance of incongruence. Cladistics 10, 315–319.
| Crossref | GoogleScholarGoogle Scholar |
Felsenstein J.
(1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Crossref | GoogleScholarGoogle Scholar |
Frati F.,
Simon C.,
Sullivan J., Swofford D. L.
(1997) Evolution of the mitochondrial cytochrome oxidase II gene in Collembola. Journal of Molecular Evolution 44, 145–158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hecker K. H., Roux K. H.
(1996) High and low annealing temperatures increase both specificity and yield in “Touchdown” and “StepDown” PCR. BioTechniques 20, 478–485.
| PubMed |
Hennig W.
(1965) Vorarbeiten zu einem phylogenetischen System der Muscidae (Diptera: Cyclorrhapha). Stuttgarter Beitrage zur Naturkunde 141, 000–000.
Holt R. A.,
Subramanian G. M.,
Halpern A.,
Sutton G. G.,
Charlab R.,
Nusskern D. R., Wincker P. , et al..
(2002) The genome sequence of the malaria mosquito Anopheles gambiae. , 129–149.
| Crossref | GoogleScholarGoogle Scholar |
Howland D. E., Hewitt G. M.
(1995) Phylogeny of the Coleoptera based on mitochondrial cytochrome oxidase I sequence data. Insect Molecular Biology 4, 203–215.
| PubMed |
Huelsenbeck J. P., Rannala B.
(1997) Phylogenetic methods come of age: testing hypothesis in an evolutionary context. Science 276, 227–232.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huelsenbeck J. P., Ronquist F.
(2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Johnson K. P.,
Moylet R. G.,
Witt C. C.,
Faucett R. C., Weckstein J. D.
(2001) Phylogenetic relationships in the louse genus Penenirmus based on nuclear (EF-1α) and mitochondrial (COI) DNA sequences. Systematic Entomology 26, 491–497.
| Crossref | GoogleScholarGoogle Scholar |
Kluge A. G.
(1989) A concern for evidence and a phylogenetic hypothesis for relationships among Epicrates (Boidae, Serpentes). Systematic Zoology 38, 7–25.
| Crossref | GoogleScholarGoogle Scholar |
Kluge A. G., Wolf A. J.
(1993) Cladistics: what’s in a word? Cladistics 9, 183–199.
| Crossref | GoogleScholarGoogle Scholar |
Lemmon A. R., Moriarty E. C.
(2004) The importance of proper model assumption in bayesian phylogenetics. Systematic Biology 53, 265–277.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lessinger A. C.,
Martins Junqueira A. C.,
Lemos T. A.,
Kemper E. L.,
da Silva F. R.,
Vettore A. L.,
Arruda P., Azeredo-Espin A. M. L.
(2000) The mitochondrial genome of the primary screwworm fly Cochliomyia homnivorax (Diptera: Calliphoridae). Insect Molecular Biology 9, 521–529.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu H., Beckenbach A. T.
(1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Molecular Phylogenetics and Evolution 1, 41–52.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Méier R., Wiegmann B. M.
(2002) A phylogenetic analysis of Coelopidae (Diptera) based on morphological and DNA sequence data. Molecular Phylogenetics and Evolution 25, 393–407.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Michelsen V.
(1991) Revision of the aberrant New World genus Coenosopsia (Diptera: Anthomyiidae), with a discussion of anthomyiid relationships. Systematic Entomology 16, 85–104.
Mitchell A.,
Cho S.,
Regier J. C.,
Mitter C.,
Poole R. W., Matthews M.
(1997) Phylogenetic utility of elongation factor-1α in Noctuoidea (Insecta: Lepidoptera): the limits of synonymous substitution. Molecular Biology and Evolution 14, 381–390.
| PubMed |
Miyamoto M. M., Fitch W. M.
(1995) Testing species phylogenies and phylogenetic methods with congruence. Systematic Biology 44, 64–76.
| Crossref | GoogleScholarGoogle Scholar |
Motta H. C. G., Couri M. S.
(1999) Revisão das espécies de Bithoracochaeta Stein (Diptera, Muscidae). Revista Brasileira de Zoologia 16, 665–689.
Moulton J. K., Wiegmann B. M.
(2004) Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged Eremoneuran Diptera (Insecta). Molecular Phylogenetics and Evolution 31, 363–378.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nihei S. S., Carvalho C. J. B. de
(2004) Taxonomy, cladistics and biogeography of Coenosopsia Malloch (Diptera, Anthomyiidae) and its significance to the evolution of anthomyiids in the Neotropics. Systematic Entomology 29, 260–275.
| Crossref | GoogleScholarGoogle Scholar |
Pamplona D. M.
(1986) Revalidação de Biopyrellia Townsend, 1932 com redescrição de B. bipuncta (Wiedemann, 1830) (Diptera, Muscidae, Muscinae). Revista Brasileira de Biologia 46, 49–54.
Pamplona D. M.
(1999) Nova caracterização de Cyrtoneurina Giglio-Tos, 1893 e descrição de Paracyrtoneurina g.n. (Diptera, Muscidae). Revista Brasileira de Entomologia 43, 9–24.
Pont A. C., Carvalho C. J. B.
(1997) Three new species of Muscidae (Diptera) from Dominican amber. Studia Dipterologica 4, 173–181.
Posada D., Crandall K. A.
(1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roback S. S.
(1951) A classification of the muscoid calyptrate Diptera. Annals of the Entomological Society of America 44, 327–361.
Rokas A.,
Nylander J. A. A.,
Ronquist F., Stone G. N.
(2002) A maximum-likelihood analysis of eight phylogenetic markers in gallwasps (Hymenoptera: Cynipidae): implications for insect phylogenetic studies. Molecular Phylogenetics and Evolution 22, 206–219.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Savage J., Wheeler T. A.
(2004) Phylogeny of the Azeliini (Diptera: Muscidae). Studia Dipterologica 11, 259–299.
Savage J.,
Wheeler T. A., Wiegmann B. M.
(2004) Phylogenetic analysis of the genus Thricops Rondani (Diptera: Muscidae) based on molecular and morphological characters. Systematic Entomology 29, 395–414.
| Crossref | GoogleScholarGoogle Scholar |
Scheffer S., Wiegmann B. M.
(2000) Molecular phylogenetics of the holly leafminers (Diptera: Agromyzidae: Phytomyza): species limits, speciation, and dietary specialization. Molecular Phylogenetics and Evolution 17, 244–255.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schmidt H. A.,
Strimmer K.,
Vingron M., von Haeseler A.
(2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schuehli G. S., Carvalho C. J. B. de
(2005) Revision and cladistics of the Neotropical genus Pseudoptilolepis Snyder, (Diptera: Muscidae). Revista Brasileira de Zoologia 22, 23–34.
| Crossref | GoogleScholarGoogle Scholar |
Schuehli G. S.,
Carvalho C. J. B. de, Wiegmann B. M.
(2004) Regarding the taxonomic status of Ophyra Robineau-Desvoidy (Diptera: Muscidae): a molecular approach. Zootaxa 712, 1–12.
Sharpe R. G.,
Harbach R. E., Butlin R. K.
(2000) Molecular variation and phylogeny of members of the Mimus group of Anopheles subgenus Cellia (Diptera: Culicidae). Systematic Entomology 25, 263–272.
| Crossref | GoogleScholarGoogle Scholar |
Simon C.,
Frati F.,
Beckenbach A.,
Crespi B.,
Liu H., 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.
Smith S. W.,
Overbeek R.,
Woese C. R.,
Gilbert W., Gillevet P. M.
(1994) The genetic data enviroment and expandible GUI for multiple sequence analysis. Computer Applications in the Biosciences 10, 671–675.
| PubMed |
Snyder F. M.
(1954) A revision of Cyrtoneurina Giglio-Tos, with notes on related genera (Diptera, Muscidae). Bulletin of the American Museum of Natural History 103, 417–464.
Soares E. D. G., Carvalho C. J. B. de
(2005) Taxonomia, análise cladística e descrição de uma espécie nova de Palpibracus Rondani (Diptera, Muscidae). Revista Brasileira de Entomologia 49, 171–180.
| Crossref | GoogleScholarGoogle Scholar |
Sperling F. A. H., Hickey D. A.
(1994) Mitochondrial DNA sequence variation in the spruce budworm species complex (Choristoneura: Lepidoptera). Molecular Biology and Evolution 11, 656–665.
| PubMed |
Sperling F. A. H.,
Anderson G. S., Hickey D. A.
(1994) A DNA-based approach to the identification of insect species used for postmortem interval estimation. Journal of Forensic Sciences 39, 418–427.
| PubMed |
Strimmer K., von Haeseler A.
(1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964–969.
Swofford D. L.,
Waddell P. J.,
Huelsenbeck J. P.,
Foster P. G.,
Lewis P. O., Rogers J. S.
(2001) Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Systematic Biology 50, 525–539.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang L.,
Wiegmann B. M.,
Yeates D. K., Irwin M. E.
(2000) Higher-level phylogeny of the Therevidae (Diptera: Insecta) based on 28s ribosomal and Elongation Factor-1α gene sequences. Molecular Phylogenetics and Evolution 15, 440–451.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yeates D. K., Wiegmann B. M.
(1999) Congruence and controversy: toward a higher-level phylogeny of Diptera. Annual Review of Entomology 44, 397–428.
| Crossref | GoogleScholarGoogle Scholar | PubMed |