Eur. J. Entomol. 112 (1): 165-174, 2015 | DOI: 10.14411/eje.2015.007

Morphological and molecular characterization of common European species of Adialytus (Hymenoptera: Braconidae: Aphidiinae) based on the mtCOI barcoding gene and geometric morphometrics of forewings

Saša S. STANKOVIĆ1, Andjeljko PETROVIĆ2, Marijana ILIĆ MILOŠEVIĆ1, Petr STARÝ3, Nickolas G. KAVALLIERATOS4, Vladimir ŽIKIĆ1, Željko TOMANOVIĆ2
1 Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000 Niš, Serbia; e-mails: sasasta@gmail.com; marijanailic83@yahoo.com; zikicvladimir@gmail.com
2 Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia; e-mails: andjeljko@bio.bg.ac.rs; ztoman@bio.bg.ac.rs
3 Institute of Entomology, Biology Centre, Czech Academy of Sciences, Branišovská 31, 37005 České Budějovice, Czech Republic; e-mail: stary@entu.cas.cz
4 Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 Stefanou Delta str., Kifissia, 14561, Attica, Greece; e-mail: nick_kaval@hotmail.com

In this study three common European species of the genus Adialytus Förster, 1862 were examined: Adialytus ambiguus (Haliday, 1834), Adialytus salicaphis (Fitch, 1855) and Adialytus thelaxis (Starý, 1961). Molecular analysis involved the DNA barcoding of a region of the mitochondrial gene cytochrome oxidase I (COI). The genetic difference based on Kimura s two-parameter model for computing pairwise distances showed that A. thelaxis differs from both A. ambiguus and A. salicaphis by 4.9 and 6% on average, respectively. The genetic distance between A. ambiguus and A. salicaphis was 1.5% on average, suggesting that barcodes based on the COI gene are insufficiently informative for separating these two species. Geometric morphometrics analysis of forewing size and shape revealed statistically significant differences. The R1 vein on the forewing of A. ambiguus is more elongated than on the wings of A. salicaphis and A. thelaxis. The geometric morphometrics analysis of the forewings also revealed that A. salicaphis and A. thelaxis have much broader forewings, suggesting strong flight ability associated with their parasitizing arboricolous aphids. The distal part of the forewing of Adialytus ambiguus is narrower, which in this case suggests poor flight ability associated with parasitizing Sipha aphids on grasses. An illustrated key for identifying the European species of Adialytus is provided.

Keywords: Hymenoptera, Braconidae, Adialytus, parasitoids, morphology, genetic diversity, key

Received: February 11, 2014; Revised: July 25, 2014; Accepted: July 25, 2014; Prepublished online: October 16, 2014; Published: January 25, 2015  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
STANKOVIĆ, S.S., PETROVIĆ, A., ILIĆ MILOŠEVIĆ, M., STARÝ, P., KAVALLIERATOS, N.G., ŽIKIĆ, V., & TOMANOVIĆ, Ž. (2015). Morphological and molecular characterization of common European species of Adialytus (Hymenoptera: Braconidae: Aphidiinae) based on the mtCOI barcoding gene and geometric morphometrics of forewings. EJE112(1), 165-174. doi: 10.14411/eje.2015.007
Download citation

References

  1. Baylac M., Villemant C. & Simbolotti G. 2003: Combining geometric morphometrics with pattern recognition or the investigation of species complexes. - Biol. J. Linn. Soc. 80: 89-98 Go to original source...
  2. Bookstein F.L. 1991: Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, New York, 435 pp Go to original source...
  3. Bookstein F.L. 1997: Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. - Med. Image Anal. 1: 225-243 Go to original source...
  4. Culliney T.W., Nagamine W.T. & Teramoto K.K. 2003: Introductions for biological control in Hawaii 1997-2001. - Proc. Hawaiian Entomol. Soc. 36: 145-153
  5. Derocles S.A., Le Ralec A., Plantegenest M., Chaubet B., Cruaud C., Cruaud A. & Rasplus J.Y. 2012: Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). - Mol. Ecol. Resour. 12: 197-208 Go to original source...
  6. 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. - Mol. Mar. Biol. Biotechnol. 3: 294-299
  7. Foerster A. 1862: Synopsis der Familien und Gattungen der Braconiden. - Verh. Naturh. Ver. Preuss. Rheinl. 19: 225-288
  8. Gahan A.B. 1910: Some synonymy and other notes on Aphidiinae. - Proc. Entomol. Soc. Wash. 12: 179-189
  9. Godfray H.C.J. 1994: Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton, 488 pp Go to original source...
  10. Hagvar E.B. & Hofsvang T. 1991: Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control. - Biocontr. News Inform. 12: 13-41
  11. Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003: Biological identifications through DNA barcodes. - Proc. R. Soc. Lond. (B) 270: 313-321 Go to original source...
  12. Kavallieratos N.G., Tomanovic Z., Stary P., Athanassiou C.G., Sarlis G.P., Petrovic O., Niketic M. & Veroniki M.A. 2004: A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant association. - Appl. Entomol. Zool. 39: 527-563 Go to original source...
  13. Kavallieratos N.G., Tomanovic Z., Stary P., Zikic V. & Petrovic-Obradovic O. 2010: Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Solanaceae and Cucurbitaceae crops in Southeastern Europe: Aphidiine-aphid-plant associations and key. - Ann. Entomol. Soc. Am. 103: 153-164 Go to original source...
  14. Kim D.W., Yoo W.G., Park H.C., Yoo H.S., Kang D.W., Jin S.D., Min H.K., Paek W.K. & Lim J. 2012: DNA barcoding of fish, insects, and shellfish in Korea. - Genomics Inform. 10: 206-211 Go to original source...
  15. Klingenberg C.P. 2011: MorphoJ: An integrated software package for geometric morphometrics. - Mol. Ecol. Resour. 11: 353-357 Go to original source...
  16. Mackauer M. 1968: Pars 3. Aphidiidae. In Ferriere C. & van der Vecht J. (eds): Hymenopterorum Catalogus (nova edito). Dr. W. Junk, The Hague, 103 pp
  17. Mackauer M. & Stary P. 1967: World Aphidiidae. Index of Entomophagous Insects. Le Francois, Paris, 195 pp
  18. Mescheloff E. & Rosen D. 1990: Biosystematic studies on the Aphidiidae of Israel (Hymenoptera: Ichneumonoidea) 3. TheGenera Adialytus and Lysiphlebus. - Isr. J. Entomol. 24: 35-50
  19. Michelena J.M., Gonzalez P. & Soler E. 2004: Parasitoides afdiinos (Hymenoptera, Braconidae, Aphidiinae) de pulgones de cultivos agricolas en la Comunidad Valenciana. - Bol. San. Veg. Plagas 30: 317-326
  20. Mitrovski-Bogdanovic A., Petrovic A., Mitrovic M., Ivanovic A., Zikic V., Stary P., Vorburger C. & Tomanovic Z. 2013: Identification of two cryptic species within the Praon abjectum group (Hymenoptera: Braconidae: Aphidiinae) using molecular markers and geometric morphometrics. - Ann. Entomol. Soc. Am. 106: 170-180 Go to original source...
  21. Packer L., Gibbs J., Sheffield C. & Hanner R. 2009: DNA barcoding and the mediocrity of morphology. - Mol. Ecol. Resour. (Suppl. 1) 9: 42-50 Go to original source...
  22. Pennacchio F. & Tremblay E. 1986: Biosystematic and morphological study of two Aphidius ervi Haliday (Hymenoptera: Braconidae) biotypes with the description of a new species. - Boll. Lab. Entomol. Agr. Filippo Silvestri 43: 105-117
  23. Petrovic A., Tomanovic Z. & Zikic V. 2006: Wahlgreniella ossiannilssoni Hille Ris Lambers, a new host for Aphidius microlophii Pennacchio and Tremblay (Hymenoptera: Braconidae: Aphidiinae). - Arch. Biol. Sci. 58: 41-42 Go to original source...
  24. Petrovic A., Mitrovic M., Stary P., Petrovic-Obradovic O., Zikic V., Tomanovic Z. & Vorburger C. 2013: Lysiphlebus orientalis (Hymenoptera, Braconidae), a new invasive aphid parasitoid in Europe - evidence from molecular markers. - Bull. Entomol. Res. 103: 451-457 Go to original source...
  25. Pike K.S., Stary P., Miller T., Graf G., Allison D., Boydston L. & Miller R. 2000: Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northwest USA. - Proc. Entomol. Soc. Wash. 102: 688-740
  26. Quicke D.L.J. & Belshaw R. 1999: Incongruence between morphological data sets: An example from the evolution of endoparasitism among parasitic wasps (Hymenoptera: Braconidae). - Syst. Biol. 48: 436-454 Go to original source...
  27. Rakhshani E., Stary P. & Tomanovic Z. 2012: Species of Adialytus Foerster, 1862 (Hymenoptera, Braconidae, Aphidiinae) in Iran: taxonomic notes and tritrophic associations. - ZooKeys 221: 81-95 Go to original source...
  28. Rodriguez F.A., Rojas S.F., Lizarde K.L. & Stary P. 2001: Internacion a Chile de Adialytus salicaphis (Hym.: Aphidiidae), parasitoide del pulgon del alamo Chaitophorus leucomelas Koch (Hem.: Aphididae). In: Proceedings of XXIII Congr. Nac. de Entomologia, 5-7 Dec. 2001, Temuco, Chile. Sociedad Chilena de Entomologia y Facultad de Ciencias Agronomicas de la Universidad de la Frontera
  29. Rohlf F.J. 2005: TpsDig, Digitize Landmarks and Outlines, version 2.05. Department of Ecology and Evolution. State University of New York at Stony Brook (http://life.bio.sunysb.edu/morph/)
  30. Rohlf F.J. & Slice D.E. 1990: Extensions of the Procrustes method for the optimal superimposition of landmarks. - Syst. Zool. 39: 40-59 Go to original source...
  31. Sandrock C., Schirrmeister B. & Vorburger C. 2011: Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. - BMC Evol. Biol. 11: 348 Go to original source...
  32. Sharkey M.J. & Wharton R.A. 1997: Morphology and terminology. In Wharton R.A., Marsh P.M. & Sharkey M.J. (eds): Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special publication 1, International Society of Hymenopterists, Washington, DC, pp. 19-37
  33. Sheets H.D. 2003: IMP Suite (Integrated Morphometrics Package). Canisius College, Buffalo, NY
  34. Shujauddin 1978: New record of Adialytus Foerster (Hymenoptera: Aphidiidae) from India with comments on the validity of the genus. - J. Entomol. Res. 2: 160-162
  35. Smith C.F. 1944: The Aphidiinae of North America (Braconidae: Hymenoptera). Ohio State University, Columbus, 153 pp
  36. Stankovic S.S., Stary P. & Mifsud D. 2013: Aphids and their parasitoids on the Canary grass, Phalaris canariensis in Malta (Hymenoptera, Braconidae, Aphidiinae). - Bull. Entomol. Soc. Malta 6: 137-141
  37. Stary P. 1970: Biology of Aphid Parasites (Hymenoptera: Aphidiidae) with Respect to Integrated Control. Dr. W. Junk, The Hague, 643 pp
  38. Stary P. 1975: The subgeneric classification of Lysiphlebus Forster 1862. - Annot. Zool. Bot. Bratislava 105: 1-9
  39. Stary P. 1979: Aphid Parasites (Hymenoptera, Aphididae) of the Central Asian Area. Dr. W. Junk, The Hague, 105 pp Go to original source...
  40. Stary P. 2006: Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae: Aphidiinae). Academia, Praha, 430 pp
  41. Stary P. & Juchnevic L.A. 1978: Aphid parasites (Hymenoptera: Aphidiidae) from Kazakhstan, USSR. - Pol. J. Entomol. 48: 523-532 Go to original source...
  42. Stary P. & Pike K.S. 1999: Uses of beneficial insect diversity in agroecosystem management. Chapter 4. In Collins W.W. & Qualset C.O. (eds): Biodiversity in Agroecosystems. CRC Press, Boca Raton, FL, pp. 49-67 Go to original source...
  43. Stary P. & Rakauskas R.P. 1979: Adialytus balticus sp.n., a parasitoid of Dysaphis anthrisci from the east Baltic (Hymenoptera, Aphidiidae; Homoptera, Aphididae). - Acta. Entomol. Bohemoslov. 76: 313-317
  44. Stary P. & Schlinger E.S. 1967: A Revision of the Far East Asian Aphidiidae (Hymenoptera). Dr. W. Junk, The Hague, 204 pp Go to original source...
  45. Takada H. 1968: Aphidiidae of Japan (Hymenoptera). - Insecta Matsumur. 30: 67-124
  46. Takada H. 1979: Aphidiidae (Hymenoptera) from Mongolia. - Folia Entomol. Hung. 32: 189-202
  47. Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739 Go to original source...
  48. Tomanovic Z., Kavallieratos N.G., Stary P., Stanisavljevic L., Petrovic-Obradovic O., Tomanovic S. & Jovanovic S. 2006: Aphids and parasitoids on willows and poplars in southeastern Europe (Hemiptera: Aphidoidea; Hymenoptera: Braconidae, Aphidiinae). - J. Plant Dis. Prot. 113: 174-180 Go to original source...
  49. Tomanovic Z., Kos K., Petrovic A., Stary P., Kavallieratos N.G., Zikic V., Jakse J., Trdan S. & Ivanovic A. 2013: The relationship between molecular variation and variation in the wing shape of three aphid parasitoid species: Aphidius uzbekistanicus Luzhetzki, Aphidius rhopalosiphi De Stefani Perez and Aphidius avenaphis (Fitch) (Hymenoptera: Braconidae: Aphidiinae). - Zool. Anz. 252: 41-47 Go to original source...
  50. Tremblay E. & Pennacchio F. 1988: Speciation in Aphidiinae (Hymenoptera). In Gupta V.K. (eds): Advances in Parasitic Hymenoptera Research. E.J. Brill, New York, pp. 139-146
  51. Zelditch M.L., Swiderski D.L., Sheets H.D. & Fink W.L. 2004: Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, New York, pp. 443
  52. Zikic V., Tomanovic Z., Ivanovic A., Kavallieratos N.G., Stary P., Stanisavljevic L. & Rakhshani E. 2009: Morphological characterization of Ephedrus persicae biotypes (Hymenoptera: Braconidae: Aphidiinae) in the Palaearctic. - Ann. Entomol. Soc. Am. 102: 1-11 Go to original source...
  53. Zikic V., Ilic Milosevic M., Stankovic S., Petrovic A., Petrovic-Obradovic O., Kavallieratos N.G., Stary P. & Tomanovic Z. 2012: Aphidiinae (Hymenoptera: Braconidae) of Serbia and Montenegro - tritrophic interactions. - Acta Entomol. Serb. 17: 83-105
  54. Zurovcova M., Havelka J., Stary P., Vechtova P., Chundelova D., Jarosova A. & Kucerova L. 2010: "DNA barcoding" is of limited value for identifying adelgids (Hemiptera: Adelgidae) but supports traditional morphological taxonomy. - Eur. J. Entomol. 107: 147-156 Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.