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

Monophyly and phylogenetic relationships of Thereva and therevine genus-groups (Insecta : Diptera : Therevidae) based on EF-1α, 28S rDNA and mitochondrial 16S rDNA sequences

Kevin C. Holston A D , Michael E. Irwin B and Brian M. Wiegmann C
+ Author Affiliations
- Author Affiliations

A Department of Entomology, Swedish Museum of Natural History, Stockholm, Sweden.

B Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana-Champaign, IL 61801, USA.

C Department of Entomology, North Carolina State University, Raleigh, North Carolina, USA.

D Corresponding author. Email: kevin.holston@nrm.se

Invertebrate Systematics 21(3) 279-296 https://doi.org/10.1071/IS06005
Submitted: 8 February 2006  Accepted: 4 May 2007   Published: 27 June 2007

Abstract

Phylogenetic analyses using 28S rDNA, elongation factor (EF)-1α, and mt 16S rDNA sequences were performed to test the monophyly of Thereva Latreille. Two of the three Afrotropical Thereva species groups lack the genitalia characters that unambiguously diagnose Thereva in the Holarctic Region, but phylogenetic relationships among Thereva species groups and therevine genera are poorly understood. Using an extensive taxonomic sample (39 of the 62 therevine genera) and Thereva, sensu lato (15 spp.), simultaneous analyses of all three gene partitions recovered Nearctic and Palaearctic Thereva species in a well supported clade that includes the Afrotropical seminitida-group but excludes the Afrotropical analis- and turneri-groups. Stronger phylogenetic signal from the EF-1α partition, measured by the skewness statistic and proportion of total parsimony informative characters, dominated conflicting signal from the 16S partition and weaker, but more congruent, signal from 28S. Reducing the taxonomic sample in analyses of Therevinae reduced homoplasy, increased phylogenetic structure and partitioned Bremer support values and reduced incongruence with 28S for the 16S partition. Although molecular analyses yielded partial recovery of informal therevine genus-groups, morphological diagnoses of higher-level groups are poorly supported with the exception of Cyclotelini. The ‘Holarctic radiation’ refers to a diverse clade of genera closely related to Pandivirilia Irwin & Lyneborg and Acrosathe Irwin & Lyneborg widely distributed throughout the Holarctic Region that is the sister-group to Thereva, sensu stricto. Results from these analyses underscore the importance of male and female genitalia characters in recognising monophyletic groups and regional endemism in therevine diversification.


Acknowledgements

We are grateful to the following collectors for providing specimens for this study: Daniel Bennett, Chris Dietrich, Martin Hauser, Christian Kassebeer, Ray Miller, J. Kevin Moulton, Manfred Niehuis, Frank Parker, Evert I. Schlinger, Christian Schmid-Egger, Karel Spitzer, Shaun L. Winterton and Chen Young. We thank Kristin M. Algmin, Brian Cassel, Hilary Hill and Gail E. Kampmeier for logistical and technical support. Comments from Stewart Berlocher, Stephen D. Gaimari, Martin Hauser, Chris Lambkin, Mark Metz, Donald W. Webb, James B. Whitfield, Shaun L. Winterton and an anonymous reviewer on earlier versions of this manuscript are greatly appreciated. This paper is based on dissertational research by the first author at the University of Illinois at Urbana-Champaign, Illinois, and the support and encouragement of May Berenbaum and other members of the Department of Entomology is greatly appreciated. Financial support for this research was provided by the Schlinger Foundation and the National Science Foundation (DEB-9521925 and DEB-9977958). Any opinions, findings, and conclusions or recommendations expressed in this paper are those of the authors and do not necessarily reflect the views of the National Science Foundation.


References


Báez M. (1982) Dípteros de Canarias IX: Therevidae. Boletin de la Asociacion Espanola de Entomologia 6, 79–99. open url image1

Baker R. H., DeSalle R. (1997) Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Systematic Biology 46, 674–698.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 | open url image1

Barker F. K., Lutzoni F. M. (2002) The utility of the incongruence length difference test. Systematic Biology 51, 625–637.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Black W. C., Piesman J. (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proceedings of the National Academy of Sciences of the United States of America 91, 10034–10038.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bremer K. (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42, 795–803.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bremer K. (1994) Branch support and tree stability. Cladistics 10, 295–304.
Crossref | GoogleScholarGoogle Scholar | open url image1

Broughton R. E., Cott S., Stanley E., Durrett R. T. (2000) Quantification of homoplasy for nucleotide transitions and transversions and a reexamination of assumptions in weighted phlyogenetic analyses. Systematic Biology 49, 617–627.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. open url image1

Burk A., Douzery J. P., Springer M. S. (2002) The secondary structure of mammalian mitochondrial 16S rRNA moleculas: refinements based on a comparative phylogenetic approach. Journal of Mammalian Evolution 9, 225–252.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caterino M. S., Cho S., Sperling F. A. H. (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annual Review of Entomology 45, 1–54.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chirgwin J. M., Przbyla A. E., MacDonald R. J., Rutter W. J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294–5299.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cho S., Mitchell A., Regier J. C., Mitter C., Poole R. W., 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 |
open url image1

Cruickshank R. H. (2002) Molecular markers for the phylogenetics of mites and ticks. Systematic and Applied Acarology 7, 3–14. open url image1

Cunningham C. W. (1997) Can three incongruence tests predict when data should be combined? Molecular Biology and Evolution 14, 733–740.
PubMed |
open url image1

Darlu P., Lecointre G. (2002) When does the incongruence length difference test fail? Molecular Biology and Evolution 19, 432–437.
PubMed |
open url image1

Dolphin K., Belshaw R., Orme C. D. L., Quicke D. L. J. (2000) Noise and incongruence: Interpreting results of the incongruence length difference test. Molecular Phylogenetics and Evolution 17, 401–406.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Farris J. S., Källersjö M., Kluge A. G., Bult C. (1994) Testing significance of incongruence. Cladistics 10, 315–319.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farris J. S., Källersjö M., Kluge A. G., Bult C. (1995) Constructing a significance test for incongruence. Systematic Biology 44, 570–572.
Crossref | GoogleScholarGoogle Scholar | open url image1

Felsenstein J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gaimari S.D., Irwin M.E. (2000) Phylogeny, classification, and biogeography of the cycloteline Therevinae (Insecta: Diptera: Therevidae). Zoological Journal of the Linnaean Society 129, 129–240.
Crossref |
open url image1

Hamby R. K., Sims L., Issel L., Zimmer E. (1988) Direct ribosomal RNA sequencing: optimization of extraction and sequencing methods for work with higher plants. Plant Molecular Biology Reporter 6, 175–192. open url image1

Hancock J. M., Tautz D., Dover G. A. (1988) Evolution of the secondary structures and compensatory mutations to the ribosomal RNAs of Drosophila melanogaster. Molecular Biology and Evolution 5, 393–414.
PubMed |
open url image1

Hauser M., Irwin M. E. (2003) The Nearctic genus Ammonaios Irwin and Lyneborg 1981 (Diptera: Therevidae). Annals of the Entomological Society of America 96, 738–765.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hillis D. M., Hulsenbeck J. P. (1992) Signal, noise, and reliability in molecular phylogenetic analyses. The Journal of Heredity 83, 189–195.
PubMed |
open url image1

Hipp A. L., Hall J. C., Systma K. J. (2004) Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. Systematic Biology 53, 81–89.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Holston K. C. (2004) A systematic database of Thereva Latreille names: an answer to the nomenclatural challenge in Therevidae (Insecta: Diptera). Memoirs of the American Entomological Society 45, 1–86. open url image1

Holston K. C., Irwin M. E. (2005) Revision of the Nearctic Thereva (Diptera: Asiloidea: Therevidae). Studia Dipterologica Supplement 13, 1–219. open url image1

Irwin M.E., Lyneborg L. (1981) The genera of Nearctic Therevidae. Illinois Natural History Survey Bulletin 32, 193–277. open url image1

Källersjö M., Albert V. A., Farris J. S. (1999) Homoplasy increases phylogenetic structure. Cladistics 15, 91–93. open url image1

Lamb T., Bauer A. M. (2001) Mitochondrial phylogeny of Namib day geckos (Rhoptropus) based on cytochrome b and 16S rRNA sequences. Copeia 2001, 775–780.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lambkin C. L. (2004) Partitioned Bremer support localises significant conflict in bee flies (Diptera: Bombyliidae; Anthracinae). Invertebrate Systematics 18, 351–360.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lyneborg L. (1976) A revision of the therevine stiletto-flies (Diptera: Therevidae) of the Ethiopian Region. Bulletin of the British Museum (Natural History) – Entomology 33, 189–346. open url image1

Lyneborg L. (1983a) A review of the Palaearctic genera of Phycinae (Insecta, Diptera, Therevidae). Steenstrupia 9, 181–205. open url image1

Lyneborg L. (1983b) The west Mediterranean genus Chrysanthemyia Becker (Insecta, Diptera, Therevidae). Steenstrupia 9, 77–82. open url image1

Lyneborg L. (1986a) Genera of Therevidae new to the Palaearctic Region (Insecta, Diptera, Therevidae). Steenstrupia 12, 61–71. open url image1

Lyneborg L. (1986b) The Palaearctic species of Pandivirilia Irwin and Lyneborg, 1981 (Insecta, Diptera, Therevidae). Steenstrupia 12, 85–98. open url image1

Lyneborg L. (1986c) The genus Acrosathe Irwin and Lyneborg, 1981 in the Old World (Insecta, Diptera, Therevidae). Steenstrupia 12, 101–113. open url image1

Lyneborg L. (1987) A remarkable new Thereva Latreille from Tunisia (Diptera: Therevidae). Annals of the Natal Museum 28, 463–465. open url image1

Lyneborg L. (1989) Iberotelus, a new genus of Therevidae (Diptera) from Spain. Eos Revista Española de Entomologia 64, 89–94. open url image1

Lyneborg L. (1992) Therevidae (Insecta: Diptera). Fauna of New Zealand 24, 3–137. open url image1

Lyneborg L. (2001) The Australian stiletto flies of the Anabaryhnchus genus-group (Diptera: Therevidae). Entomonograph 13, 1–256. open url image1

Lyneborg L., Zaitzev V. F. (1980) Hoplosathe, a new genus of palaearctic Therevidae (Diptera), with description of six new species. Entomologica Scandinavica 11, 81–93. open url image1

Maddison D. R., and Maddison W. P. (2005). ‘MacClade: Analysis of Phylogeny and Character Evolution. Version 4.0.’ (Sinauer: Sunderland, MA.)

Mardulyn P. A., Whitfield J. B. (1999) Phylogenetic signal in the COI, 16S, and 28S genes for inferring relationships among genera of Microgastrinae (Hymenoptera; Braconidae): evidence of a high diversification rate in this group of parasitoids. Molecular Phylogenetics and Evolution 12, 282–294.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Metz M. A., Irwin M. E. (2000) Revision of Lindneria Kröber, with the description of two new genera Insulatitan and Ambradolon, a fossil from Dominican amber (Diptera: Therevidae: Therevinae). Annals of the Entomological Society of America 93, 977–1018.
Crossref | GoogleScholarGoogle Scholar | open url image1

Metz M. A., Webb D. W., Irwin M. E. (2003) A review of the genus Psilocephala Zetterstedt (Diptera: Therevidae) with the description of four new genera. Studia Dipterologica 10, 227–266. open url image1

Nagatomi A., Lyneborg L. (1988) The Japanese Acrosathe (Diptera, Therevidae). Kontyû 56, 600–617. open url image1

Nagatomi A., Nagatomi T. S. H., Lyneborg L. (1991) Apsilocephalidae, a new family of the Orthorrhaphous Brachycera (Insecta, Diptera). Zoological Science 8, 579–591. open url image1

Pollock D. D., Zwickl D. J., McGuire J. A., Hillis D. M. (2002) Increased taxonomic sampling is advantageous for phylogenetic inference. Systematic Biology 51, 664–671.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Remsen J., O’Grady P. (2002) Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Molecular Phylogenetics and Evolution 24, 249–264.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanmartín I., Ronquist F. (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53, 216–243.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanmartín I., Enghoff H., Ronquist F. (2001) Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnaean Society 73, 345–390.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schmitz J., Moritz R. F. A. (1998) Molecular phylogeny of Vespidae (Hymenoptera) and the evolution of sociality in wasps. Molecular Phylogenetics and Evolution 9, 183–191.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith S. D., Bond J. E. (2003) An analysis of the secondary structure of the mitochondrial large subunit rRNA gene (16S) in spiders and its implications forphylogenetic reconstruction. The Journal of Arachnology 31, 44–54.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sorenson M. D. (1999). ‘TreeRot, Version 2.’ (Boston University: Boston, MA, USA.)

Staden R. (1996) The Staden sequence analysis package. Molecular Biotechnology 5, 233–241.
PubMed |
open url image1

Swofford D. L. (1999). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods).’ Version 4. (Sinauer: Sunderland, MA, USA.)

Webb D. W. (2005a) A revision of the Holarctic genus Spiriverpa Irwin and Lyneborg (Diptera: Therevidae: Therevinae). Zootaxa 816, 1–56. open url image1

Webb D. W. (2005b) Revision of the Neotropical stiletto fly genus Notiothereva Metz and Irwin (Diptera: Therevidae: Therevinae). Zootaxa 1059, 1–32. open url image1

Webb D. W., Irwin M. E. (1991a) The Nearctic genus Nebritus Coquillett (Diptera: Therevidae: Therevinae). Proceedings of the Entomological Society of Washington 93, 899–913. open url image1

Webb D. W., Irwin M. E. (1991b) The North American genus Megalinga Irwin and Lyneborg (Diptera: Therevidae: Therevinae). Proceedings of the Entomological Society of Washington 93, 914–924. open url image1

Webb D. W., Irwin M. E. (1999) Revision of Tabuda Walker and Tabudamima Irwin and Lyneborg, with the description of a new genus Incoxoverpa Webb and Irwin (Diptera: Therevidae: Therevinae). Annals of the Entomological Society of America 92, 644–674. open url image1

Webb D. W., Metz M. A. (2003a) The Nearctic species of Pandivirilia Irwin and Lyneborg (Diptera: Therevidae: Therevinae). Annals of the Entomological Society of America 96, 369–402.
Crossref | GoogleScholarGoogle Scholar | open url image1

Webb D. W., Metz M. A. (2003b) The South American genus Protothereva Malloch (Diptera: Therevidae: Therevinae) with description of two new species. Zootaxa 234, 1–12. open url image1

Whiting M. F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winterton S. L., Irwin M. E., Yeates D. K. (1999) Phylogenetic revision of the Taenogera Kröber genus-group (Diptera: Therevidae), with descriptions of two new genera. Australian Journal of Entomology 38, 274–290.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winterton S. L., Yang L., Wiegmann B. M., Yeates D. K. (2001) Phylogenetic revision of Agapophytinae subf.n. (Diptera: Therevidae) based on molecular and morphological evidence. Systematic Entomology 26, 173–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Woodley N. E. (1989). Phylogeny and classification of the ‘Orthorraphous’ Brachycera. In ‘Manual of Nearctic Diptera’. (Ed. J. F. McAlpine.) pp. 1371–1395 (Research Branch Agriculture Canada: Ottawa.)

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 | open url image1

Yeates D. K. (1992) Towards a monophyletic Bombyliidae (Diptera): the removal of the Proratinae (Diptera: Scenopinidae). American Museum Novitates 3051(30), 1–30. open url image1

Yeates D. K. (2002) Relationships of extant lower Brachycera (Diptera): a quantitative synthesis of morphological characters. Zoologica Scripta 31, 105–121.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yeates D. K., Irwin M. E., Wiegmann B. M. (2003) Ocoidae, a new family of asiloid flies (Diptera: Brachycera: Asiloidea), based on Ocoa chilensis gen. and sp.n. from Chile, South America. Systematic Entomology 28, 417–431.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yoder A. D., Irwin J. A., Paysuer B. A. (2001) The failure of the ILD to determine data combinability for slow loris phylogeny. Systematic Biology 50, 408–424.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zwickl D. J., Hillis D. M. (2002) Increased taxonomic sampling greatly reduces phylogenetic error. Systematic Biology 51, 588–598.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1