Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-13T06:58:54.518Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular species delimitation in the genus Eumerus (Diptera: Syrphidae)

Published online by Cambridge University Press:  30 August 2016

A. Chroni ,
M. Djan ,
D. Obreht Vidaković ,
T. Petanidou  and
A. Vujić
A. Chroni*
Affiliation:
Department of Geography, University of the Aegean, University Hill, 81100, Mytilene, Greece
M. Djan
Affiliation:
Faculty of Sciences, Department of Biology and Ecology, University of Novi Sad, Trg Dositeja Obradovića 3, 2100, Novi Sad, Serbia
D. Obreht Vidaković
Affiliation:
Faculty of Sciences, Department of Biology and Ecology, University of Novi Sad, Trg Dositeja Obradovića 3, 2100, Novi Sad, Serbia
T. Petanidou
Affiliation:
Department of Geography, University of the Aegean, University Hill, 81100, Mytilene, Greece
A. Vujić
Affiliation:
Faculty of Sciences, Department of Biology and Ecology, University of Novi Sad, Trg Dositeja Obradovića 3, 2100, Novi Sad, Serbia
*
*Author for correspondence Phone: +302251036423 Fax: +302251036423 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Eumerus is one of the most diverse genera of hoverfly worldwide. Species delimitation within genus is considered to be difficult due to: (a) lack of an efficient key; (b) non-defined taxonomical status of a large number of species; and (c) blurred nomenclature. Here, we present the first molecular study to delimit species of the genus by using a fragment of the mitochondrial cytochrome-c oxidase subunit I gene (COI) gene. We assessed 75 specimens assigned to 28 taxa originating from two biogeographic zones: 22 from the western Palaearctic and six from the Afrotropical region. Two datasets were generated based on different sequence lengths to explore the significance of availability of more polymorphic sites for species delimitation; dataset A with a total length of 647 bp and dataset B with 746 bp. Various tree inference approaches and Poisson tree processes models were applied to evaluate the putative ‘taxonomical’ vs. ‘molecular’ taxa clusters. All analyses resulted in high taxonomic resolution and clear species delimitation for both the dataset lengths. Furthermore, we revealed a high number of mitochondrial haplotypes and high intraspecific variability. We report two major monophyletic clades, and seven ‘molecular’ groups of taxa formed, which are congruent with morphology-based taxonomy. Our results support the use of the mitochondrial COI gene in species diagnosis of Eumerus.

Keywords

DNA barcodingCOIspecies KeyDelimitationhoverfliesEumerus
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 1 , February 2017 , pp. 126 - 138
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahrens, D., Fujisawa, T., Krammer, H.J., Eberle, J., Fabrizi, S. & Vogler, A.P. (2016) Rarity and incomplete sampling in DNA-based species delimitation. Systematic Biology 65 (3), 478–494.CrossRefGoogle ScholarPubMed
Avise, J. (2000) Phylogeography: The History and Formation of Species. Masahousette, Harvard University Press.CrossRefGoogle Scholar
Ball, S.L., Hebert, P.D.N., Burian, S.K. & Webb, J.M. (2005) Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. Journal of the North American Benthological Society 24, 508–524.CrossRefGoogle Scholar
Bandelt, H.J., Forster, P., Sykes, B.C. & Richards, M.B. (1995) Mitochondrial portraits of human populations using median networks. Genetics 141, 743–753.CrossRefGoogle ScholarPubMed
Bandelt, H.J., Forster, P. & Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Bergsten, J. (2005) A review of long-branch attraction. Cladistics 21, 163–193.CrossRefGoogle ScholarPubMed
Buhay, J.E. (2009) ‘Coi-Like’ sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29, 96–110.CrossRefGoogle Scholar
Chen, H., Rangasamy, M., Tan, S.Y., Wang, H.C. & Siegfried, B.D. (2010) Evaluation of five methods for total DNA extraction from western corn rootworm beetles. PLoS ONE 5(8), 1–6.Google ScholarPubMed
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.CrossRefGoogle Scholar
DeWalt, R.E. (2011) DNA barcoding: a taxonomic point of view. Journal of the North American Benthological Society 30, 174–181.CrossRefGoogle Scholar
Doczkal, D. & Pape, T. (2009) Lyneborgimyia magnifica gen. et sp.n. (Diptera: Syrphidae) from Tanzania, with a phylogenetic analysis of the Eumerini using new morphological characters. Systematic Entomology 34 (3), 559–573.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Francuski, L., Djurakic, M., Ludoški, J. & Milankov, V. (2013) Landscape genetics and spatial pattern of phenotypic variation of Eristalis tenax across Europe. Journal of Zoological Systematics and Evolutionary Research 51, 227–238.CrossRefGoogle Scholar
Gibson, J.F., Kelso, S., Jackson, M.D., Kits, J.H., Miranda, G.F.G. & Skevington, J.H. (2011) Diptera-specific polymerase chain reaction amplification primers of use in molecular phylogenetic research. Annals of the Entomological Society of America 104, 976–997.CrossRefGoogle Scholar
Goloboff, P. (1999) NONA (no name). Version 2. Published by the Author, Tucuman, Argentina.Google Scholar
Haarto, A. & Ståhls, G. (2014) When mtDNA COI is misleading: congruent signal of ITS2 molecular marker and morphology for North European Melanostoma Schiner, 1860 (Diptera, Syrphidae). ZooKeys 431, 93–134.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003 a) Biological identifications through DNA barcodes. Proceedings of the Royal Society B – Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Ratnasingham, S. & deWaard, J.R. (2003 b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B – Biological Sciences 270, S96–S99.CrossRefGoogle ScholarPubMed
Hebert, P.D.N. & Gregory, T.R. (2005) The promise of DNA barcoding for taxonomy. Systematic Biology 54, 852–859.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., deWaard, J.R. & Landry, J.F. (2010) DNA barcodes for 1/1000 of the animal kingdom. Biology Letters 6, 359–362.CrossRefGoogle ScholarPubMed
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Jordaens, K., Goergen, G., Virgilio, M., Backeljau, T., Vokaer, A. & De Meyer, M. (2015) DNA barcoding to improve the taxonomy of the Afrotropical Hoverflies (Insecta: Diptera: Syrphidae). PLoS ONE 10(10), e0140264.CrossRefGoogle ScholarPubMed
Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.CrossRefGoogle ScholarPubMed
Leasi, F. & Norenburg, J.L. (2014) The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS ONE 9, e104385.CrossRefGoogle ScholarPubMed
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Maddison, W.P. & Maddison, D.R. (2011) Mesquite: a Modular System for Evolutionary Analysis. Version 3.03. Available online at http://mesquiteproject.org Google Scholar
Marcos-García, M.Á., Vujić, A., Ricarte, A. & Ståhls, G. (2011) Towards an integrated taxonomy of the Merodon equestris species complex (Diptera: Syrphidae) including description of a new species, with additional data on Iberian Merodon. Entomological Society of Canada 143, 332–348.CrossRefGoogle Scholar
Mengual, X., Ståhls, G., Vujić, A. & Marcos-García, M.Á. (2006) Integrative taxonomy of Iberian Merodon species (Diptera, Syrphidae). Zootaxa 1377, 1–26.Google Scholar
Milankov, V., Stamenković, J., Ludoški, J., Ståhls, G. & Vujić, A. (2005) Diagnostic molecular markers and the genetic relationships among three species of the Cheilosia canicularis group (Diptera: Syrphidae). European Journal of Entomology 102, 125–131.CrossRefGoogle Scholar
Milankov, V., Ståhls, G., Stamenković, J. & Vujić, A. (2008 a) Genetic diversity of populations of Merodon aureus and M. cinereus species complexes (Diptera, Syrphidae):integrative taxonomy and implications for conservation priorities on the Balkan Peninsula. Conservation Genetics 9, 1125–1137.CrossRefGoogle Scholar
Milankov, V., Ståhls, G. & Vujić, A. (2008 b) Molecular diversity of populations of the Merodon ruficornis group (Diptera, Syrphidae) on the Balkan Peninsula. Journal of Zoological Systematics and Evolutionary Research 46, 143–152.CrossRefGoogle Scholar
Milankov, V., Ludoški, J., Ståhls, G., Stamenković, J. & Vujić, A. (2009) High molecular and phenotypic diversity in the Merodon avidus complex (Diptera, Syrphidae): cryptic speciation in a diverse insect taxon. Biological Journal of the Linnean Society 155, 819–833.CrossRefGoogle Scholar
Milankov, V., Francuski, L., Ludoški, J., Ståhls, G. & Vujić, A. (2010 a) Estimating genetic and phenotypic diversity in a northern hoverfly reveals lack of heterozygosity correlated with significant fluctuating asymmetry of wing traits. Journal of Insect Conservation 14, 77–88.CrossRefGoogle Scholar
Milankov, V., Francuski, L., Ludoški, J., Ståhls, G. & Vujić, A. (2010 b) Genetic structure and phenotypic diversity of two northern populations of Cheilosia aff. longula (Diptera: Syrphidae) has implications for evolution and conservation. European Journal of Entomology 107, 305–315.CrossRefGoogle Scholar
Milankov, V., Ludoški, J.L.F., Ståhls, G. & Vujić, A. (2013) Genetic and phenotypic diversity patterns in Merodon albifrons Meigen, 1822 (Diptera: Syrphidae): evidence of intraspecific spatial and temporal structuring. Biological Journal of the Linnean Society 110, 257–280.CrossRefGoogle Scholar
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees, pp. 1–8 in Gateway Computing Environments Workshop (GCE), New Orleans, LA.CrossRefGoogle Scholar
Moritz, C. & Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology 2, 1529–1531.CrossRefGoogle ScholarPubMed
Nedeljković, Z., Ačanski, J., Vujić, A., Obreht, D., Dan, M., Ståhls, G. & Radenković, S. (2013) Taxonomy of Chrysotoxum festivum Linnaeus, 1758 (Diptera: Syrphidae) – an integrative approach. Zoological Journal of the Linnean Society 169, 84–102.CrossRefGoogle Scholar
Nedeljković, Z., Ačanski, J., Dan, M., Obreht-Vidaković, D., Ricarte, A. & Vujić, A. (2015) An integrated approach to delimiting species borders in the genus Chrysotoxum Meigen, 1803 (Diptera: Syrphidae), with description of two new species. Contributions to Zoology 84(4), 285–304.CrossRefGoogle Scholar
Nixon, K.C. (2002) WINCLADA ver. 1.00.08. New York, University of Ithaca.Google Scholar
Pape, T. & Thompson, F.C. (Eds) 2015. Systema Dipterorum. Version 1.5. Available online at http://www.diptera.org/ (accessed 18 September 2015).Google Scholar
Peck, L.V. (1988) Syrphidae, pp. 11–230 in Soos, A. & Papp, L. (Eds) Catalogue of Palaearctic Diptera. Budapest, Akaddémiai Kiadó.Google Scholar
Pérez-Bañón, C., Rojo, S., Ståhls, G. & Marcos-García, M.Á. (2003) Taxonomy of European Eristalinus (Diptera: Syrphidae) based on larval morphology and molecular data. European Journal of Entomology 100, 417–428.CrossRefGoogle Scholar
Petanidou, T., Ståhls, G., Vujić, A., Olesen, J.M., Rojo, S., Thrasyvoulou, A., Sgardelis, S., Kallimanis, A.S., Kokkini, S. & Tscheulin, T. (2013) Investigating plant-pollinator relationships in the Aegean: the approaches of the project POL-AEGIS (The pollinators of the Aegean archipelago: diversity and threats). Journal of Apicultural Research 52(2), 106–117.CrossRefGoogle Scholar
Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (2001) Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580–601.CrossRefGoogle ScholarPubMed
Radenković, S., Vujić, A., Ståhls, G., Pérez-Bañón, C., Rojo, S., Petanidou, T. & Simić, S. (2011) Three new cryptic species of the genus Merodon Meigen (Diptera: Syrphidae) from the island of Lesvos (Greece). Zootaxa 2735, 35–56.CrossRefGoogle Scholar
Rodriguez, F., Oliver, J.L., Marin, A. & Medina, J.R. (1990) The general stochastic-model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.CrossRefGoogle ScholarPubMed
Rotheray, G.E. & Gilbert, F. (2011) The Natural History of Hoverflies. UK, Ceredigion.Google Scholar
Rubinoff, D. (2006) Utility of mitochondrial DNA barcodes in species conservation. Conservation Biology 20, 1026–1033.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Smith, M.A., Fisher, B.L. & Hebert, P.D.N. (2005) DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society B – Biological Sciences 360, 1825–1834.CrossRefGoogle Scholar
Soldati, L., Kergoat, G.J., Clamens, A.L., Jourdan, H., Jabbour-Zahab, R. & Condamine, F.L. (2014) Integrative taxonomy of New Caledonian beetles: species delimitation and definition of the Uloma isoceroides species group (Coleoptera, Tenebrionidae, Ulomini), with the description of four new species. Zookeys 415, 133–167.Google Scholar
Speight, M.C.D. (2014) Species accounts of European Syrphidae (Diptera). Syrph the Net, the database of European Syrphidae, vol. 78, pp. 321. Syrph the Net publications, Dublin.Google Scholar
Suk, S.W. & Han, H.Y. (2013) Clarification of previously confused Chrysotoxum sapporense and Chrysotoxum graciosum (Insecta: Diptera: Syrphidae) in East Asia based on morphological and molecular data. Animal Cells and Systems 17(4), 277–289. doi: 10.1080/19768354.2013.814588.CrossRefGoogle Scholar
Stackelberg, A.A. (1961) Palaearctic species of the genus Eumerus Mg. (Diptera, Syrphidae). Trudy vses.ent., Obshch 48, 181–229.Google Scholar
Ståhls, G., Stuke, J.H., Vujić, A., Doczkal, D. & Muona, J. (2004) Phylogenetic relationships of the genus Cheilosia and the tribe Rhingiini (Diptera, Syrphidae) based on morphological and molecular characters. Cladistics – the International Journal of the Willi Hennig Society 20, 105–122.CrossRefGoogle ScholarPubMed
Ståhls, G., Vujić, A. & Milankov, V. (2008) Cheilosia vemalis (Diptera, Syrphidae) complex: molecular and morphological variability. Annales Zoologici Fennici 45, 149–159.CrossRefGoogle Scholar
Ståhls, G., Vujić, A., Pérez-Bañón, C., Radenković, S., Rojo, S. & Petanidou, T. (2009) COI barcodes for identification of Merodon hoverflies (Diptera, Syrphidae) of Lesvos Island, Greece. Molecular Ecology Resources 9, 1431–1438.CrossRefGoogle ScholarPubMed
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.CrossRefGoogle ScholarPubMed
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.CrossRefGoogle ScholarPubMed
Tang, C.Q., Humphreys, A.M., Fontaneto, D. & Barraclough, T.G. (2014) Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data. Methods in Ecology and Evolution 5, 1086–1094.CrossRefGoogle ScholarPubMed
Thompson, F.C., Rotheray, G.E. & Zimbado, M.A. (2010) Syrphidae (flower flies), pp. 763–792 in Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, Norman, E. & Zumbado, M.A. (Eds) Manual of Central American Diptera. Ottawa, NRC Research Press.Google Scholar
Vujić, A., Radenković, S., Ståhls, G., Ačanski, J., Stefanović, A., Veselić, S., Andrić, A. & Hayat, R. (2012) Systematics and taxonomy of the ruficornis group of genus Merodon Meigen (Diptera: Syrphidae). Systematic Entomology 37, 578–602.CrossRefGoogle Scholar
Vujić, A., Ståhls, G., Ačanski, J., Bartsch, H., Bygebjerg, R. & Stefanović, A. (2013) Systematics of Pipizini and taxonomy of European Pipiza Fallen: molecular and morphological evidence (Diptera, Syrphidae). Zoologica Scripta 42, 288–305.CrossRefGoogle Scholar
Young, A.D., Marshall, S.A. & Skevington, J.H. (2016) Revision of Platycheirus Lepeletier and Serville (Diptera: Syrphidae) in the Nearctic north of Mexico. Zootaxa 4082(1), 001–317.CrossRefGoogle ScholarPubMed
Zhang, J.J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.CrossRefGoogle ScholarPubMed
Supplementary material: File

Chroni supplementary material

Table S1

Download Chroni supplementary material(File)
File 35.4 KB
Supplementary material: PDF

Chroni supplementary material

Table 1

Download Chroni supplementary material(PDF)
PDF 143.9 KB
Supplementary material: PDF

Chroni supplementary material

Table 2

Download Chroni supplementary material(PDF)
PDF 169.9 KB
Supplementary material: PDF

Chroni supplementary material

Table 3

Download Chroni supplementary material(PDF)
PDF 157.4 KB
Supplementary material: PDF

Chroni supplementary material

Table 4

Download Chroni supplementary material(PDF)
PDF 161.5 KB