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Molecular systematics and taxonomy of hoverflies (Diptera, Syrphidae) and related groups

Gunilla Ståhls

Molecular data, and DNA sequence data in particular, is a useful tool for studies on different aspects of organismal biology, and their potential for the study of insect biodiversity, systematics and evolution is immense. The application of DNA sequences (including the “DNA barcode”) advances our knowledge of the biology of cyclorraphan fly groups in a multitude of ways e.g. by discovering cryptic species, supplementing the description of species new to science, or associating different life stages. DNA-based methods firmly anchored within a traditional taxonomic framework have the potential to provide both a reliable, accurate identification of the species as well as taxonomy of target organisms. The molecular data utilized for this purpose is routinely collected from at least two unlinked sources (mitochondrial and nuclear) for all taxa of the current studies, to be analysed and interpreted in conjunction with morphological characters and species ecology.

The gene regions for studies on closely related insect species include the mitochondrial cytochrome c oxidase subunit I (COI), the nuclear second spacer region (Internal Transcribed Spacer 2, ITS2), while for higher level systematic studies also the nuclear ribosomal 18S and 28S rRNA gene regions are sequenced. Presently, studies on the phylogenetic relationships of many genera and tribes of Syrphidae using both morphological and molecular characters are in process. Phylogenetic analyses mostly include both morphological and molecular character sets and are conducted using standard parsimony (e.g. NONA) and/or the optimisation alignment program POY vs. 4.

Ongoing projects

Syrphidae: taxonomy and systematics of tribe Pipizini

The taxonomy of genera Pipiza and Heringia (tribe Pipizini) in Europe remains incomplete.  In Fennoscandia at least eight Pipiza species occur that in most cases can be morphologically distinguished using a combination of morphological characters. P. noctiluca has been treated as a species-complex in its present sense, and at present only the males of genus Heringia can be reliably determined to species. The ongoing studies aim to combine DNA sequence characters and extended morphological character studies with studies of all available type materials of Pipiza and Heringia with the aim of establishing species limits of European species, to link the male with female sex in cases in unclear cases and to identify and link unknown immature stages with the generated DNA sequences of adult specimens/species.

Applying molecular characters to elucidate species delimitation and/or detect morphologically cryptic species is one of the most useful applications of DNA sequences, and applied to long-standing “problem” taxa is most useful for the syrphid scientific community. Project collaborators: prof. Ante Vujic (Serbia), Hans Bartsch (Sweden), Rune Bygebjerg (Sweden).

Syrphidae: Biodiversity and phylogeography of Merodon spp. in the Eastern Aegean (Greece).

The Greek Eastern Aegean islands have habitats with a rich geophyte flora facilitating life history studies of this hoverfly taxon. The studies on Merodon spp in the Eastern Aegean include comparison of species biodiversity, mitochondrial haplotype diversity and adult morphological variability of Merodon species/populations from target islands in the Eastern Aegean. High Merodon species diversity in the Mediterranean may be linked to narrow host specificity, but tests are complicated by still incomplete taxonomy of the flies and unknown immature food sources (host plants). The phylogenetic diversity of the island faunas will be contrasted with samples from the Greek mainland. Project collaborators: prof. Ante Vujić (Serbia), prof. Vesna Milankov (Serbia), prof. Santos Rojo (Spain), Dr. Celeste Perea-Banon and prof. Theodora Petanidou (Greece).

Fig 2. Merodon pruni, female.

Platypezidae: ecology and faunistics

Flat-footed flies, Platypezidae, are principally forest dwelling species, and dependent on decaying wood as substrate for lignicolous fungi in which larvae develop as endobionts, inhabiting both soft and hard fruit bodies of various fungi. The genus Callomyia presents a different feeding mode in which larvae are obligatory epibionts (feeding type is micromycophagy), developing on the mycelium film under the bark on decaying wood or on fungal growth on the surface of other fungi. The species number for Finland is currently 30 (Ståhls, unpublished).

The genus Agathomyia is the most diverse genus of the family with 12 species recorded from Finland, and the immature biology is unknown for 6 species. Adult specimens of Agathomyia spp. are almost exclusively collected in old decidious woodland habitat, with a good amount of dead wood present. The known species of Agathomyia develop internally in polypore fungi.

Using DNA characters to link unknown immature stages of platypezids will speed up rate of discovery, and facilitate unambiguous species assignments as the obtained DNA sequence data has showed that species possess diverse and unique species specific sequences.

Fig. 3. Paraplatypeza atra.

Publications in International refereed journals last 5 years

  • Milankov, V., Francuski, Lj., Ludoški, J., Ståhls, G., Vujic, A. 2010: 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.
  • Milankov, V., Francuski, Lj., Ludoški, J., Ståhls, G., Vujic, A. 2010: 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.
  • Ståhls, G. & Vujić, A. 2009: Cryptopipiza notabila (Violovitsh, 1985) (Diptera, Syrphidae) new to Finland. Sahlbergia 15(2):1-2.
  • Mengual, X., Ruiz, C., Rojo, S., Ståhls, G. & Thompson, F.C. 2009: A conspectus of the flower fly genus Allograpta (Diptera: Syrphidae) with description of a new subgenus and species. Zootaxa 2214: 1-28.
  • Ståhls, G., Vujić, A., Pérez-Bañon, 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.
  • Milankov, V. Ludoski, J., Ståhls, G., Stamenkovic, J. & Vujic, 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 155: 818-833.
  • Mengual, X., Ståhls, G. & Rojo, S. 2008: Molecular phylogeny of Allograpta (Diptera, Syrphidae) reveals diversity of lineages and non-monophyly of phytophagous taxa. Molecular Phylogenetics and Evolution 49: 715-727.
  • Milankov, V., Ståhls, G., Stamenkovic, J. & Vujić, A. 2008: 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.
  • Mengual, X., Ståhls, G. & Rojo, S. 2008: First phylogeny of predatory flowerflies (Diptera, Syrphidae, Syrphinae) using mitochondrial COI and nuclear 28S rRNA genes: conflict and congruence with the current tribal classification. Cladistics, 24: 543-562.
  • Mikkola, K. & Ståhls, G. 2008: Morphological and molecular taxonomy of Dendrolimus sibiricus Chetverikov stat rev. and allied lappet moths (Lepidoptera, Lasiocampidae), with descriptions of a new species. Entomologica Fennica 19: 65-85.
  • Ståhls, G., Milankov, V. & Vujić, A.2008: Genetic diversity and phylogenetic relationships of the Cheilosia vernalis-melanura group. Annales Zoologici Fennici 45: 149-159.
  • Milankov, V., Ståhls, G. & Vujić, A. 2008: 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.
  • Vujić, A., Ståhls, G., Rojo, S., Radenković, S., & Simić, S. 2008: Systematics and phylogeny of the tribe Paragini (Diptera, Syrphidae) based on molecular and morphological characters. Zoological Journal of the Linnean Society 152: 506-536.
  • Milankov, V., Ståhls, G. & Vujić, A. 2008: Genetic characterization of the Balkan endemic species Merodon desuturinus (Diptera, Syrphidae). European Journal of Entomology 105: 197-204.
  • Ståhls, G. & Savolainen, E. 2007: MtDNA COI barcodes reveal cryptic diversity in the Baetis vernus group (Ephemeroptera, Baetidae). Molecular Phylogenetics and Evolution 46: 82-87.
  • Kehlmaier, C. & Ståhls, G. 2007: Finnish Pipunculidae (Diptera) studies part II: an annotated checklist of Finnish big-headed flies. Sahlbergia 13: 44-68.
  • Vujić, A., Pérez-Bañón, C., Radenković, S., Ståhls, G., Rojo, S., Petanidou, T., and Simić, S. 2007: Two new species of Merodon Meigen, 1803 (Syrphidae, Diptera) from the island of Lesvos (Greece), East Mediterranean. Ann. Soc. Entomol. France 43: 319-326.
  • Skevington, J., Kehlmaier, C. & Ståhls, G. 2007: Molecular barcoding: Mixed results for big-headed flies (Diptera: Pipunculidae). Zootaxa 1423: 1-26.
  • Lawrence, J. E., Muona, J., Teräväinen, M., Ståhls, G. & Vahtera, V. 2007: Anischia, Perothops and the phylogeny of Elateroidea (Coleoptera: Elateriformia). Insect Systematics and Evolution 38: 205-239.
  • Ståhls, G. & Kahanpää, J. 2006: New data on Platypezidae and Opetiidae (Diptera) of Finland. Sahlbergia, 11: 1-6.
  • Ståhls, G. 2006: Placement of Cacoceria and phylogenetic relationships of the xylotine genera of the tribe Milesiini (Diptera, Syrphidae: Eristalinae) based on molecular characters. Zootaxa, 1171: 17-29.
  • Laska, P., Perez-Banon, C., Mazanek, L., Rojo, S., Ståhls, G., Marcos-Garcia, M.A., Bicik, V. & Dusek, J. 2006: Taxonomy of the genera Scaeva, Simosyrphus and Ischiodon (Diptera: Syrphidae): Descriptions of immature stages and status of taxa. European Journal of Entomology103: 637–655.
  • Kaila, L. & Ståhls, G. 2006: DNA barcodes: Evaluating the potential of COI in delimitation of closely related species of Elachista (Lepidoptera: Gelechioidea: Elachistidae) from Australia. Zootaxa, 1170: 1-26.
  • Mengual, X., Ståhls, G., Vujic, A. & Marcos-Garcia, M. A. 2006: Integrative taxonomy of Iberian Merodon species (Diptera, Syrphidae). Zootaxa 1377: 1-26.
  • Rojo, S., Ståhls, G., Perez-Banon, C., & Marcos-Garcia, M. A. 2006: Taxonomic identity of the Holarctic Paragus sg. Pandasyopthalmus species (Diptera, Syrphidae) based on larval and molecular characters. European Journal of Entomology, 103: 443-458.