Skip to main content
SpringerLink
Log in

An integrative approach in the assessment of species delimitation and structure of the Merodon nanus species group (Diptera: Syrphidae)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

The Merodon nanus group (Diptera, Syrphidae) is a small group of closely related species with high morphological similarity. Until now, based on morphological characters, this group consisted of five species: M. nanus Sack, 1931; M. telmateia Hurkmans, 1987; M. kopensis Vujić et Hayat, 2015; M. neonanus Vujić et Taylor, 2015; and M. rasicus Vujić et Radenković, 2015. Here, using an integrative approach based on molecular characters (sequences of the D2–3 region of the nuclear 28S rRNA gene and the mitochondrial COI gene) and data obtained from geometric morphometry of wing shape, we distinguish all five previously morphologically defined species of the group. Additionally, we identify one species as being new to science, M. vladimiri Vujić et Kočiš Tubić sp. n. We emphasize the separation of this newly described species according to the sequences obtained from the slowly evolving 28S rRNA gene, which demonstrated four to five mutation positions between this species and morphologically the most similar M. neonanus species. Also, our results show a clear division of M. telmateia into at least three population groups that we designate as the subspecies: M. telmateia mediterraneus Ačanski et Kočiš Tubić subsp. n. and M. telmateia samosensis Ačanski et Kočiš Tubić subsp. n. exhibiting western distributions (western Anatolia and the Greek island of Samos, respectively) and the nominative subspecies M. telmateia telmateia with an eastern Anatolian distribution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Ačanski, J. (2017). Taxonomy and distribution of the genus Merodon Meigen (Diptera: Syrphidae) in Palearctic. PhD thesis, University of Novi Sad, 209pp.

  • Ačanski, J., Vujić, A., Djan, M., Obreht Vidaković, D., Ståhls, G., & Radenković, S. (2016). Defining species boundaries in the Merodon avidus complex (Diptera, Syrphidae) using integrative taxonomy, with the description of a new species. European Journal of Taxonomy, 237, 1–25. https://doi.org/10.5852/ejt.2016.237.

    Article  Google Scholar 

  • Arif, I. A., & Khan, H. A. (2009). Molecular markers for biodiversity analysis of wildlife animals: a brief review. Animal Biodiversity and Conservation, 32(1), 9–17.

    Google Scholar 

  • Arnqvist, G., & Mårtensson, T. (1998). Measurement error in geometric morphometrics: empirical strategies to assess and reduce its impact on measures of shape. Acta Zoologica Academiae Scientiarum Hungaricae, 44, 73–96.

    Google Scholar 

  • Baylac, M., & Frieß, M., (2005). Fourier descriptors, Procrustes superimposition, and data dimensionality: an example of cranial shape analysis in modern human populations. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 145–165).

  • Belshaw, R., Lopez-Vaamonde, C., Degerli, N., & Quicke, D. L. J. (2001). Paraphyletic taxa and taxonomic chaining: evaluating the classification of braconine wasps (Hymenoptera: Braconidae) using 28S D2-3 rDNA sequences and morphological characters. Biological Journal of the Linnean Society, 73, 411–424. https://doi.org/10.1006/bijl.2001.0539.

    Article  Google Scholar 

  • Betts, C. R., & Wootton, R. J. (1988). Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. Journal of Experimental Biology, 138, 271–288.

    Google Scholar 

  • Birdsall, K., Zimmerman, E., Teeter, K., & Gibson, G. (2000). Genetic variation for the positioning of wing veins in Drosophila melanogaster. Evolution and Development, 2, 16–24.

    CAS  PubMed  Google Scholar 

  • Bitner-Mathé, B. C., & Klaczko, B. L. (1999). Size and shape heritability in natural populations of Drosophila mediopunctata: temporal and microgeographical variation. Genetica, 105, 35–42.

    PubMed  Google Scholar 

  • Bluemel, J. K., Derlink, M., Pavlovčič, P., Russo, I.–. R. M., Andrew King, R., Corbett, E., Sherrard-Smith, E., Blejec, A., Wilson, M. R., Stewart, A. J. A., Symondson, W. O. C., & Virant-Doberlet, M. (2014). Integrating vibrational signals, mitochondrial DNA and morphology for species determination in the genus Aphrodes (Hemiptera: Cicadellidae). Systematic Entomology, 39, 304–324.

    Google Scholar 

  • Caterino, M. S., & Tishechkin, A. K. (2006). DNA identification and morphological description of the first confirmed larvae of Heteriinae (Coleoptera: Histeridae). Systematic Entomology, 31, 405–418.

    Google Scholar 

  • Chen, H., Rangasamy, M., Tan, S. Y., Wang, H., & Siegfried, B. D. (2010). Evaluation of five methods for total DNA extraction from western corn rootworm beetles. PLoS One, 5(8), e11963. https://doi.org/10.1371/journal.pone.0011963.

    PubMed  PubMed Central  Google Scholar 

  • Çiplak, B. (2003). Distribution of Tettigoniinae (Orthoptera, Tettigoniidae) bush-crickets in Turkey: the importance of the Anatolian Taurus Mountains in biodiversity and implications for conservation. Biodiversity and Conservation, 12, 47–64.

    Google Scholar 

  • Cowling, D. E., & Burnet, B. (1981). Courtship songs and genetic control of their acoustic characteristics in sibling species of the Drosophila melanogaster subgroup. Animal Behaviour, 29, 924–935.

    Google Scholar 

  • Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85(3), 407–415.

    Google Scholar 

  • Dell Statistica. (2015). Dell Statistica data analysis software system, version 13. Dell Inc.

  • Demirsoy, A. (1996). Genel ve Türkiye Zoocoğrafyası. Ankara: Meteksan AŞ.

    Google Scholar 

  • DeVries, P. J., Penz, C. M., & Hill, R. I. (2010). Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. Journal of Animal Ecology, 79(5), 1077–1085.

    CAS  PubMed  Google Scholar 

  • Dworkin, I., & Gibson, G. (2006). Epidermal growth factor receptor and transforming growth factor-β signaling contributes to variation for wing shape in Drosophila melanogaster. Genetics, 173, 1417–1431.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Floyd, R., Abebe, E., Papert, A., & Blaxter, M. (2002). Molecular barcodes for soil nematode identification. Molecular Ecology, 11, 839–850.

    CAS  PubMed  Google Scholar 

  • Folmer, D., Black, M. B., Hoch, W., Lutz, R. A., & Vrijehock, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    CAS  PubMed  Google Scholar 

  • Francuski, L., Ludoški, J., Vujić, A., & Milankov, V. (2009). Wing geometric morphometric inferences on species delimitation and intraspecific divergent units in the Merodon ruficornis group (Diptera, Syrphidae) from the Balkan Peninsula. Zoological Science, 26, 301–308.

    PubMed  Google Scholar 

  • Francuski, L., Ludoški, J., Vujić, A., & Milankov, V. (2011). Phenotypic evidence for hidden biodiversity in the Merodon aureus group (Diptera, Syrphidae) on the Balkan Peninsula: conservation implication. Journal of Insect Conservation, 15, 379–388.

    Google Scholar 

  • Goloboff, P. (1999). NONA computer program. Tucuman: Published by the author.

    Google Scholar 

  • Goulding, T. C., & Dayrat, B. (2016). Integrative taxonomy: ten years of practice and looking into the future. Сборник трудов Зоологического музея МГУ им. М.В. Ломоносова. Archives of Zoological Museum of Lomonosov Moscow State University, 54, 116–133.

    Google Scholar 

  • Grabow, K., & Rüppell, G. (1995). Wing loading in relation to size and flight characteristics of European Odonata. Odonatologica, 24(2), 175–186.

    Google Scholar 

  • Gül, S. (2013). Ecological divergence between two evolutionary lineages of Hyla savignyi (Audouin, 1827) in Turkey: effects of the Anatolian diagonal. Animal Biology, 63(3), 285–295.

    Google Scholar 

  • Habel, J. C., Meyer, M., El Mousadik, A., & Schmitt, T. (2008). Africa goes Europe: the complete phylogeography of the marbled white butterfly species complex Melanargia galathea/M. lachesis (Lepidoptera: Satyridae). Organisms Diversity and Evolution, 8(2), 121–129.

    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.

    CAS  Google Scholar 

  • Hesselbarth, G., Van Oorschot, H., & Wagener, S. (1995). Die Tagfalter der Türkei. Band 2. Nymphalidae. Bocholt: Selbsterverlag Sigbert Wagener.

    Google Scholar 

  • Hewitt, G. M. (2001). Speciation, hybrid zones and phylogeography or seeing genes in space and time. Molecular Ecology, 10(3), 537–549.

    CAS  PubMed  Google Scholar 

  • Hoikkala, A., Aspi, J., & Suvanto, L. (1998). Male courtship song frequency as an indicator of male genetic quality in an insect species, Drosophila montana. Proceedings of the Royal Society of London B: Biological Sciences, 265(1395), 503–508.

    CAS  Google Scholar 

  • Hurkmans, W. (1987). Merodon telmateia, a new hoverfly from Turkey (Diptera: Syrphidae). Entomologische Berichten (Amsterdam), 45, 69–70.

  • Hwang, U. W., & Kim, W. (1999). General properties and phylogenetic utilities of nuclear ribosomal DNA and mitochondrial DNA commonly used in molecular systematic. Korean Journal of Parasitology, 37(4), 215–228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khaghaninia, S., Jafarlu, M., Khiaban, N. G., & Askari, O. (2010). Introduction to hover flies (Diptera: Syrphidae) of sunflower and pumpkin fields in West Azerbaijan Province-Iran. Munis Entomology & Zoology Journal, 5, 270–277.

    Google Scholar 

  • Klingenberg, C. P. (2011). MORPHOJ: an integrated software package for geometric Morphometrics. Ver.2. 0. [Computer software and manual]. Molecular Ecology Resources, 11, 353–357.

    PubMed  Google Scholar 

  • Kölliker-Ott, U. M., Blows, M. W., & Hoffmann, A. A. (2003). Are wing size, wing shape and asymmetry related to field fitness of Trichogramma egg parasitoids? Oikos, 100(3), 563–573.

    Google Scholar 

  • Kosswig, C. (1995). Zoogeography of the Near East. Systematic Biology, 4(2), 49–73. https://doi.org/10.2307/sysbio/4.2.49.

    Article  Google Scholar 

  • Kustov, S. Y. (2003). Zoogeographical analysis of the hoverfly fauna (Diptera, Syrphidae) of the northwestern Caucasus. Entomological Review, 86, 188–196.

    Google Scholar 

  • Lumaret, J.-P., & Lobo, J. M. (1996). Geographic distribution of endemic dung beetles (Coleoptera, Scarabaeoidea) in the Western Palaearctic region. Biodiversity Letters, 3, 192–199.

    Google Scholar 

  • Mantel, N. A. (1976). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.

    Google Scholar 

  • Marcos-García, M. Á., Vujić, A., & Mengual, X. (2007). Revision of Iberian species of the genus Merodon (Diptera: Syrphidae). European Journal of Entomology, 104, 531–572.

    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. Canadian Entomology, 143, 332–348.

    Google Scholar 

  • Markmann, M., & Tautz, D. (2005). Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal signature sequences. Philosophical Transactions of the Royal Society B, 360, 1917–1924.

    CAS  Google Scholar 

  • Masetti, A., Luchetti, A., Sommaggio, D., Burgio, G., & Mantovani, B. (2006). Phylogeny of Chrysotoxum species (Diptera: Syrphidae) inferred from morphological and molecular characters. European Journal of Entomology, 103(2), 459–467. https://doi.org/10.14411/eje.2006.059.

    Article  CAS  Google Scholar 

  • McClain, D. K., Li, J., & Oliver Jr., J. H. (2001). Interspecific and geographical variation in the sequence of rDNA expansion segment D3 of Ixodes ticks (Acaria: Ixodidae). Heredity, 86, 234–242.

    Google Scholar 

  • Menezes, B. F., Vigoder, F. M., Peixoto, A. A., Varaldi, J., & Bitner-Mathé, B. C. (2013). The influence of male wing shape on mating success in Drosophila melanogaster. Animal Behaviour, 85(6), 1217–1223.

    Google 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 

  • Mengual, X., Ståhls, G., & Rojo, S. (2008). First phylogeny of predatory hoverflies (Diptera, Syrphidae, Syphinae) using mitochondrial COI and nuclear 28S rRNA genes: conflict and congruence with the current tribal classification. Cladistics, 24, 543–562.

    PubMed  Google Scholar 

  • Mengual, X., Ståhls, G., & Rojo, S. (2012). Is the mega-diverse genus Ocyptamus (Diptera, Syrphidae) monophyletic? Evidence from molecular characters including the secondary structure of 28S rRNA. Molecular Phylogenetics and Evolution, 62, 191–205.

    PubMed  Google Scholar 

  • Mengual, X., Ståhls, G., & Rojo, S. (2015). Phylogenetic relationships and taxonomic ranking of pipizine flower flies (Diptera: Syrphidae) with implications for the evolution of aphidophagy. Cladistics, 31, 491–508.

    PubMed  Google Scholar 

  • Mezey, J. G., & Houle, D. (2005). The dimensionality of genetic variation for wing shape in Drosophila melanogaster. Evolution, 59, 1027–1038.

    PubMed  Google Scholar 

  • Milankov, V., Ståhls, G., & Vujić, A. (2008a). Molecular diversity of populations of the Merodon ruficornis group (Diptera, Syrphidae) on the Balkan Peninsula. Journal of Zoological Systematics and Evolutionary Research, 46(2), 143–152.

    Google Scholar 

  • Milankov, V., Ståhls, G., Stamenković, J., & Vujić, A. (2008b). 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.

    Google 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. Zoological Journal of the Linnean Society London, 155, 819–833.

    Google Scholar 

  • Milankov, V., Ludoški, J., Francuski, L., 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.

    Google Scholar 

  • Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), IEEE, pp 1–8.

  • Miraldo, A., Krell, F.–. T., Smalén, M., Angus, R. B., & Roslin, T. (2014). Making the cryptic visible—resolving the species complex of Aphodius fimetarius (Linnaeus) and Aphodius pedellus (de Geer) (Coleoptera: Scarabaeidae) by three complementary methods. Systematic Entomology, 39, 531–547.

    Google Scholar 

  • Monaghan, M. T., Balke, M., Gregory, T. R., & Vogler, A. P. (2005). DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society B, 360, 1925–1933.

    CAS  Google Scholar 

  • Monteiro, F. A., Wesson, D. A., Dotson, E. M., Schofield, C. J., & Beard, C. B. (2000). Phylogeny and molecular taxonomy of the Rhodniini derived from mitochondrial and nuclear DNA sequences. American Journal of Tropical Medicine and Hygiene, 62, 460–465.

    CAS  PubMed  Google Scholar 

  • Moraes, E. M., Spressola, V. L., Prado, P. R. R., Costa, L. F., & Sene, F. M. (2004). Divergence in wing morphology among sibling species of Drosophila buzzatii cluster. Journal of Zoological Systematics and Evolutionary Research, 42, 154–158.

    Google Scholar 

  • Mutun, S. (2016). Review of oak gall wasps phylogeographic patterns in Turkey suggests a main role of the Anatolian diagonal. Turkish Journal of Forestry, 17, 1–6.

    Google Scholar 

  • Nedeljković, Z., Ačanski, J., Vujić, A., Obreht, D., Djan, 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.

    Google Scholar 

  • Nedeljković, Z., Ačanski, J., Djan, 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.

    Google Scholar 

  • Ninet, B., Jan, I., Bontems, O., Léchenne, B., Jousson, O., Panizzon, R., Lew, D., & Monod, M. (2003). Identification of dermatophyte species by 28S ribosomal DNA sequencing with a commercial kit. Journal of Clinical Microbiology, 41, 826–830.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nixon, K. C. (2002). Winclada version 1.00.08, published by author, Ithaca, New York (http://www.cladistics.com).

  • Oosterbroek, P., & Arntzen, J. W. (1992). Area-cladograms of circum-Mediterranean taxa in relation to Mediterranean palaeogeography. Journal of Biogeography, 19, 3–20.

    Google Scholar 

  • Outomuro, D., Adams, D. C., & Johansson, F. (2013). The evolution of wing shape in ornamented-winged damselflies (Calopterygidae, Odonata). Evolutionary Biology, 40, 300–309.

    Google Scholar 

  • Padial, J. M., Miralles, A., De la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, 1–14.

    Google Scholar 

  • Parks, D. H., Mankowski, T., Zangooei, S., Porter, M. S., Armanini, D. G., Baird, D. J., Langille, M. G. I., & Beiko, R. G. (2013). GenGIS 2: geospatial analysis of traditional and genetic biodiversity, with new gradient algorithms and an extensible plugin framework. PLoS One, 8(7), e69885. https://doi.org/10.1371/journal.pone.0069885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patwardhan, A., Ray, S., & Roy, A. (2014). Molecular markers in phylogenetic studies—a review. Journal of Phylogenetics & Evolutionary Biology, 2, 131. https://doi.org/10.4172/2329-9002.1000131.

    Article  CAS  Google Scholar 

  • Pérez-Bañón, C., Rojo, S., Ståhls, G., & Marcos-García, M. A. (2003). Taxonomy of European Eristalinus (Diptera: Syrphidae) based on larval morphology and molecular data. European Journal of Entomology, 100, 417–428. https://doi.org/10.14411/eje.2003.064.

    Article  Google Scholar 

  • Popović, D., Ačanski, J., Djan, M., Obreht, D., Vujić, A., & Radenković, S. (2015). Sibling species delimitation and nomenclature of the Merodon avidus complex (Diptera: Syrphidae). European Journal of Entomology, 112(4), 790–809. https://doi.org/10.14411/eje.2015.100.

    Article  Google Scholar 

  • Poulakakis, N., Kapli, P., Lymberakis, P., Trichas, A., Vardinoyiannis, K., Sfenthourakis, S., & Mylonas, M. (2015). A review of phylogeographic analyses of animal taxa from the Aegean and surrounding regions. Journal of Zoological Systematics and Evolutionary Research, 53(1), 18–32. https://doi.org/10.1111/jzs.12071.

    Article  Google Scholar 

  • Quantum GIS Development Team. (2012). Quantum GIS Geographic Information System. Version 2.12.3 Lyon [Internet]. Open Source Geospatial Foundation Project. Available: http://qgis.osgeo.org.

  • Radenković, S., Vujić, A., Ståhls, G., Perez–Banon, C., 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.

    Google Scholar 

  • Radenković, S., Šašić Zorić, L., Djan, M., Obreht Vidaković, D., Ačanski, J., Ståhls, G., Veličković, N., Markov, Z., Petanidou, T., Kočiš Tubić, N., & Vujić, A. (2018). Cryptic speciation in the Merodon luteomaculatus complex (Diptera: Syrphidae) from the eastern Mediterranean. Journal of Zoological Systematics and Evolutionary Research, 56, 170–191. https://doi.org/10.1111/jzs.12193.

    Article  Google Scholar 

  • Raupach, M. J., Astrin, J. J., Hannig, K., Peters, M. K., Stoeckle, M. Y., & Wägele, J.-W. (2010). Molecular species identification of central European ground beetles (Coleoptera: Carabidae) using nuclear rDNA expansion segments and DNA barcodes. Frontiers in Zoology, 7, 26 http://www.frontiersinzoology.com/content/7/1/26.

    PubMed  PubMed Central  Google Scholar 

  • Reemer, M., & Smit, J. (2007). Some hoverfly records from Turkey (Diptera, Syrphidae). Volucella, 8, 135–146.

    Google Scholar 

  • Ricarte, A., Nedeljković, Z., Rotheray, G. E., Yszkowski, R. M., Hancock, E. G., Watt, K., Hewitt, S. M., Horsefield, D., & Wilkinson, G. (2012). Syrphidae (Diptera) from the Greek island of Lesvos, with description of two new species. Zootaxa, 3175, 1–23.

    Google Scholar 

  • Riedel, A., Sagata, K., Suhardjono, Y. R., Tanzler, R., & Balke, M. (2013). Integrative taxonomy on the fast track—towards more sustainability in biodiversity research. Frontiers in Zoology, 10, 15.

    PubMed  PubMed Central  Google Scholar 

  • Ritchie, M. G., & Gleason, J. M. (1995). Rapid evolution of courtship song pattern in Drosophila willistoni sibling species. Journal of Evolutionary Biology, 8(4), 463–479.

    Google 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. https://doi.org/10.1016/S0022-5193(05)80104-3.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F. J. (2006). TpsDig—digitize landmarks and outlines. Ver. 2.05. [Computer software and manual] Department of Ecology and Evolution, State University of New York at Stony Brook.

  • Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.

    Google Scholar 

  • Rosenberg, M. S., & Anderson, C. D. (2011). PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods in Ecology and Evolution, 2(3), 229–232.

    Google Scholar 

  • Sacchi, R., & Hardersen, S. (2013). Wing length allometry in Odonata: differences between families in relation to migratory behaviour. Zoomorphology, 132(1), 23–32.

    Google Scholar 

  • Saribiyik, S. (2003). Milesiinae fauna of Kahramanmaraş’s Andirin town (Diptera: Syrphidae). Kastamonu Eğitim Dergisi, 11, 159–164.

    Google Scholar 

  • Šašić, L., Ačanski, J., Vujić, A., Ståhls, G., Radenković, S., Milić, D., Vidaković, D. O., & Djan, M. (2016). Molecular and morphological inference of three cryptic species within the Merodon aureus species group (Diptera: Syrphidae). PLoS One, 11(8), e0160001. https://doi.org/10.1371/journal.pone.0160001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., & Crozier, R. H. (2010). Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.

    CAS  PubMed  Google Scholar 

  • Sesli, E., & Denchev, C. M. (2008). Checklists of the myxomycetes, larger ascomycetes, and larger basidiomycetes in Turkey. Mycotaxon, 106, 65.

    Google Scholar 

  • Sfenthourakis, S. (1996). A biogeographical analysis of terrestrial isopods (Isopoda, Oniscidea) from the central Aegean islands (Greece). Journal of Biogeography, 23, 687–698. https://doi.org/10.1111/j.13652699.1996.tb00029.x.

  • Shirouzu, T., Hirose, D., & Tokumasu, S. (2007). Sequence analyses of the 28S rRNA gene D1/D2 region suggest Dacrymyces (Heterobasidiomycetes, Dacrymycetales) is polyphyletic. Mycoscience, 48, 388–394.

    CAS  Google 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.

    CAS  Google Scholar 

  • Sindaco, R., Venchi, A., Carpaneto, G. M., & Bologna, M. A. (2000). The reptiles of Anatolia: a checklist and zoogeographical analysis. Biogeographia, 21-2000, 441–554.

    Google Scholar 

  • Sonnenberg, R., Nolte, A. W., & Tautz, D. (2007). An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology, 4, 6.

    PubMed  PubMed Central  Google Scholar 

  • Ståhls, G., Hippa, H., Rotheray, G., Muona, J., & Gilbert, F. (2003). Phylogeny of Syrphidae (Diptera) inferred from combined analysis of molecular and morphological characters. Systematic Entomology, 28, 433–450.

    Google Scholar 

  • Ståhls, G., Vujić, A., Stuke, J.–. H., Doczkal, D., & Muona, J. (2004). Phylogeny of the genus Cheilosia and the tribe Rhingiini (Diptera, Syrphidae) based on molecular and morphological characters. Cladistics, 4, 1–17.

    Google Scholar 

  • Ståhls, G., Vujić, A., & Milankov, V. (2008). Cheilosia vernalis (Diptera, Syrphidae) complex: molecular and morphological variability. Annales Zoologici Fennici, 45, 149–159.

    Google 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.

    PubMed  Google Scholar 

  • Ståhls, G., Vujić, A., Petanidou, T., Cardoso, P., Radenković, S., Ačanski, J., Pérez-Bañón, C., & Rojo, S. (2016). Phylogeographic patterns of Merodon hoverflies in the eastern Mediterranean region: revealing connections and barriers. Ecology and Evolution, 6(7), 2226–2245. https://doi.org/10.1002/ece3.2021.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tauber, E., & Eberl, D. F. (2003). Acoustic communication in Drosophila. Behavioural Processes, 64(2), 197–210.

    Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weigh matrix choice. Nucleic Acids Research, 22, 4673–4680.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vitecek, S., Kučinić, M., Previšić, A., Živić, I., Stojanović, K., Keresztes, L., Bálint, M., Hoppeler, F., Waringer, J., Graf, W., & Pauls, S. U. (2017). Integrative taxonomy by molecular species delimitation: multi-locus data corroborate a new species of Balkan Drusinae microendemics. BMC Evolutionary Biology, 17, 129. https://doi.org/10.1186/s12862-017-0972-5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vujić, A., Pérez-Bañón, C., Radenković, S., Ståhls, G., Rojo, S., Petanidou, T., & Šimić, S. (2007). Two new species of the genus Merodon Meigen 1803 (Diptera: Syrphidae) from the island of Lesvos (Greece), in the eastern Mediterranean. Annales de la Société Entomologique de France (N.S.), 43(3), 319–326.

    Google Scholar 

  • Vujić, A., Marcos-García, M. Á., Saribiyik, S., & Ricarte, A. (2011). New data on the Merodon Meigen 1803 fauna (Diptera: Syrphidae) of Turkey including description of a new species and changes in the nomenclatural status of several taxa. Annales de la Société Entomologique de France (N.S.), 47, 78–88.

    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.

    Google Scholar 

  • Vujić, A., Radenković, S., Likov, L., Trifunov, S., & Nikolić, T. (2013a). Three new species of the Merodon nigritarsis group (Diptera: Syrphidae) from the Middle East. Zootaxa, 3640, 442–464.

    PubMed  Google Scholar 

  • Vujić, A., Ståhls, G., Ačanski, J., Bartsch, H., Bygebjerg, R., & Stefanović, A. (2013b). Systematics of Pipizini and taxonomy of European Pipiza Fallen: molecular and morphological evidence (Diptera, Syrphidae). Zoologica Scripta, 42, 288–305.

    Google Scholar 

  • Vujić, A., Radenković, S., Ačanski, J., Grković, A., Taylor, M., Gökhan Senol, S., & Hayat, R. (2015). Revision of the species of the Merodon nanus group (Diptera: Syrphidae) including three new species. Zootaxa, 4006(3), 439–462. https://doi.org/10.11646/zootaxa.4006.3.2.

    Article  PubMed  Google Scholar 

  • Vujić, A., Petanidou, T., Tscheulin, T., Cardoso, P., Radenković, S., Ståhls, G., Baturan, Z., Mijatović, G., Rojo, S., Perez-Banon, C., Devalez, J., Andrić, A., Jovičić, S., Krašić, D., Markov, Z., Radišić, D., & Tataris, G. (2016). Biogeographical patterns of the genus Merodon Meigen, 1803 (Diptera: Syrphidae) in islands of the eastern Mediterranean and adjacent mainland. Insect Conservation and Diversity, 9(3), 181–191. https://doi.org/10.1111/icad.12156.

    Article  Google Scholar 

  • Wang, Y., Nansen, C., & Zhang, Y. (2016). Integrative insect taxonomy based on morphology, mitochondrial DNA, and hyperspectral reflectance profiling. Zoological Journal of the Linnean Society, 177, 378–394.

    Google Scholar 

  • Will, K. W., Mishler, B. D., & Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54, 844–851.

    PubMed  Google Scholar 

  • Yeaman, S., Chen, Y., & Whitlock, M. C. (2010). No effect of environmental heterogeneity on the maintenance of genetic variation in wing shape in Drosophila melanogaster. Evolution, 64, 3398–3408.

    PubMed  Google Scholar 

  • Yildirim, E., Ljubomirov, T., & Lelej, A. S. (2014). Overview of the distribution and biogeography of Crabronidae in Turkey (Hymenoptera: Aculeata). Journal of Insect Biodiversity, 2(3), 1–27.

    Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: a primer. London: Elsevier Academic.

    Google Scholar 

  • Zohary, M. (1973). Geobotanical foundations of the Middle East (Vol. 2). Stuttgart: Gustav FischerVerlag.

    Google Scholar 

Download references

Acknowledgments

We thank John O’Brien for the English language editing.

Funding

This work was supported by the Ministry of Education, Science and Technological Development of Serbia (http://www.mpn.gov.rs/), Grant Number 173002 (Conservation strategies for the preservation of protected and strictly protected species in Serbia—hoverflies (Insecta: Diptera: Syrphidae) as model organisms).

Author information

Authors and Affiliations

  1. Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000, Novi Sad, Serbia

    Nataša Kočiš Tubić, Mihajla Djan, Ante Vujić & Snežana Radenković

  2. Zoology Unit, Finnish Museum of Natural History, University of Helsinki, PO Box 17, 00014, Helsinki, Finland

    Gunilla Ståhls

  3. BioSense Institute - Research Institute for Information Technologies in Biosystems, University of Novi Sad, Dr Zorana Đinđića 1, 21000, Novi Sad, Serbia

    Jelena Ačanski

  4. Department of Forest and Conservation Sciences, University of British Columbia, #3027 – 2424 Main Mall, Vancouver, BC, V6T 1Z4, Canada

    Dragana Obreht Vidaković

  5. Isparta, 32260, Turkey

    Rüstem Hayat

  6. Department of Plant Protection, University of Tabriz, Tabriz, 51664, Iran

    Samad Khaghaninia

Authors
  1. Nataša Kočiš Tubić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gunilla Ståhls
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jelena Ačanski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mihajla Djan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dragana Obreht Vidaković
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rüstem Hayat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Samad Khaghaninia
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ante Vujić
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Snežana Radenković
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nataša Kočiš Tubić.

Electronic supplementary material

Table S1

(DOCX 28.9 kb)

Table S2

(DOCX 15.5 kb)

Table S3

(DOCX 16.1 kb)

Fig. S1

(PDF 2204 kb)

Fig. S2

(PDF 2708 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kočiš Tubić, N., Ståhls, G., Ačanski, J. et al. An integrative approach in the assessment of species delimitation and structure of the Merodon nanus species group (Diptera: Syrphidae). Org Divers Evol 18, 479–497 (2018). https://doi.org/10.1007/s13127-018-0381-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-018-0381-7

Keywords

Search

Navigation