Jump to ContentJump to Main Navigation
Show Summary Details
More options …


More options …
Volume 71, Issue 12


High genetic diversity and a new cryptic species within the Ephedrus persicae species group (Hymenoptera: Braconidae: Aphidiinae)

Andjeljko Petrović / Korana Kocić / Katarina Kos
  • Department of Agronomy, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, SI–1111 Ljubljana, Slovenia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Milan Plećaš / Vladimir Žikić
  • Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000 Niš, Serbia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Nickolas G. Kavallieratos
  • 4Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, 75 Iera Odos str., 11855, Athens, Attica, Greece
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Željko Tomanović
  • Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-01-11 | DOI: https://doi.org/10.1515/biolog-2016-0165


In this study we used molecular markers to characterize various populations of the Ephedrus persicae species group originating from different aphid hosts and different habitat types. Twelve different haplotypes were identified in 15 E. persicae specimens, and thus there were no shared haplotypes between specimens from different aphid hosts. All haplotypes were clustered in two distinct phylogenetic clades (“persicae 1” and “persicae 2”), the average genetic distance between these two clades being 3.1%. Ephedrus persicae specimens from the “persicae 1” clade parasitize leaf-curling aphids from Prunus and Malus orchards. Furthermore, there was significant differentiation of the “persicae 2” clade into two distinct evolutionary groups, with a genetic distance of 2.5% between them. On the basis of the genetically isolated position of Ephedrus specimens associated with Brachyunguis tamaricis on Tamarix gallica (more than 5.7% genetic distance), we describe Ephedrus tamaricis sp. n. as an additional member of the E. percicae species group. Key for identification of parasitoids belonging to the E. persicae species group is provided.

Key words: Ephedrus persicae; Ephedrus tamaricis sp. n.; cytochrome oxidase subunit I; cryptic speciation


  • Akhtar M.S., Dey D. & Usmani M.K. 2011.A catalogue of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) from India. Insecta Mundi 0151: 1–31.Google Scholar

  • Belshaw R. & Quicke D.L.J. 1997. A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Mol. Phylogenet. Evol. 7 (3): 281–293. CrossrefGoogle Scholar

  • Blackman R.L. & Eastop V.F.1994. Aphids on the World’s Trees. An Identification and Information Guide. CAB International, Wallingford, 1024 pp. ISBN: 0851988776, 9780851988771Google Scholar

  • Boivin G., Hance T. & Brodeur J. 2012. Aphid parasitoids in biological control. Can. J. Plant. Sci. 92 (1): 1–12. CrossrefGoogle Scholar

  • Bribosia E., Bylemans D., Migon M. & Van Impe G. 2005. In-field production of parasitoids of Dysaphis plantaginea by using the rowan aphid Dysaphis sorbi as substitute host. BioControl 50 (4): 601–610. CrossrefGoogle Scholar

  • Carver M. & Starý P.1974. A preliminary review of the Aphidiidae (Hymenoptera: Ichneumonoidea) of Australia and New Zealand. Aust. J. Entomol. 13 (3): 235–240. CrossrefGoogle Scholar

  • Chang Y.D., Lee J.Y. & Youn Y.N. 1994. Primary parasitoids and hyperparasitoids of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Korean J. Appl. Entomol. 33 (2): 51–55.Google Scholar

  • Davidian E.M. 2007. Sem. Aphidiidae – Afidiidy [Family Aphidiidae], pp. 192–255. In: Leleϊ A.S. (ed.), Opredelitel’ nasekomykh Dal’nego Vostoka Rossii, T. 4. Setchatokryloobraznye, skorpionnidy, pereponchatokrylye, Ch. 5. [Key to the insects of the Russian Far East, Vol. 4. Neuropteroidea, Mecoptera, Hymenoptera Part 5], Dal’Nauka, Vladivostok, 1052 pp. ISBN: 978–5–8044–0789-7Google Scholar

  • Davidian E.M. & Gavrilyuk A.V. 2014. An annotated checklist of Aphidiid-wasp fauna (Hymenoptera, Aphidiidae) of Western Siberia. Entomol. Rev. 94 (6): 892–913. CrossrefGoogle Scholar

  • Derocles S.A.P., 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 (2): 197–208. .CrossrefGoogle Scholar

  • Derocles S.A.P., Plantegenest M., Rasplus J.Y., Marie A., Evans D.M., Lunt D.H. & Le Ralec A. 2016. Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes? Syst. Entomol. 41 (2): 379–391. DOI:10.1111/syen.12160CrossrefGoogle 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. Mol. Mar. Biol. Biotechnol. 3 (5): 294–299. PMID: 7881515Google Scholar

  • Gärdenfors U.1986. Taxonomic and biological revision of Palearctic Ephedrus Haliday (Hymenoptera: Braconidae, Aphidiinae). Entomol. Scand. Suppl. 27: 1–95.Google Scholar

  • Hawkins B.A. 1994. Pattern and Process in Host-Parasitoid Interactions. Cambridge University Press, Cambridge, 202 pp. ISBN: 9780521460293Google Scholar

  • Heraty J.M., Woolley J.B., Hopper K.R., Hawks D.L., Kim J.W. & Buffington M. 2007. Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Mol. Phylogenet. Evol. 45 (2): 480–493. CrossrefGoogle Scholar

  • Ilić Milošević M., Lazarević M., Petrović-Obradović O. & Žikić V. 2014. Tritrophic associations of Lysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae, Aphidiinae) in Serbia. Biologica Nyssana 5 (2): 113–121.Google Scholar

  • Kavallieratos N.G., Tomanović Ž., Petrović A., Kocic K., Jankovic M. & Starý P. 2016. Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids feeding on ornamental trees in southeastern Europe: key for identification and tritrophic associations. Ann. Entomol. Soc. Am. 109 (3): 473–487. CrossrefGoogle Scholar

  • Kavallieratos N.G., Tomanović Ž., Starý P., Athanassiou C.G., Sarlis G.P., Petrović O., Niketić M. & Anagnou-Veroniki M. 2004. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Appl. Entomol. Zoo1. 39 (3): 527–563. CrossrefGoogle Scholar

  • Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (2): 111–120. CrossrefGoogle Scholar

  • LaSalle J. & Gauld I.D. 1991. Parasitic Hymenoptera and the biodiversity crisis. Redia 74 (3) “Appendice”: 315–334.Google Scholar

  • Lumbierres B., Pons X. & Starý P. 2005. Parasitoids and predators of aphids associated with public green areas of Lleida (NE Iberian Peninsula). Adv. Hort. Sci. 19 (2): 69–75.Google Scholar

  • Mackauer M. & Starý P. 1967. World Aphidiidae (Hymenoptera, Ichneumonoidea). Index of Entomophagous Insects. Le François, Paris,195 pp.Google Scholar

  • Mifsud D., Pérez Hidalgo N. & Barbagallo S. 2009. Aphids (Hemiptera Aphidoidea) associated with native trees in Malta (Central Mediterranean). Bull. Entomol. Soc. Malta 2: 81–93.Google Scholar

  • Mitrovski-Bogdanović A., Petrović A., Mitrović M., Ivanović A., Žikić V., Starý P., Vorburger C. & Tomanović 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 (2): 170–180. CrossrefGoogle Scholar

  • Nei M. & Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, 352 pp. ISBN: 9780195135855Google Scholar

  • Ortega-Blanco J., Bennett D.J., Declos X. & Engel M.S. 2009. A primitive aphidiine wasp in Albian amber from Spain and a Northern Hemisphere origin for the subfamily (Hymenoptera: Braconidae: Aphidiinae). J. Kans. Entomol. Soc. 82 (4): 273–82. CrossrefGoogle Scholar

  • Pennacchio F. & Tremblay E. 1988. A new species of Aphidius Nees from Italy (Hymenoptera, Braconidae, Aphidiinae). Bollettino del Laboratorio di Entomologia Agraria “Filippo Silvestri” Portici 45:167–169.Google Scholar

  • Petrović A., Mitrović M., Ivanović A., Žikić V., Kavallieratos N.G., Starý P., Mitrovski-Bogdanović A., Tomanovic Z. & Vorburger C. 2015. Genetic and morphological variation in sexual and asexual parasitoids of the genus Lysiphlebus – an apparent link between wing shape and reproductive mode. BMC Evol. Biol. 15: 5. CrossrefGoogle Scholar

  • Petrović A., Mitrović M., Starý P., Petrović-Obradović O., Žikić V. & Tomanović Ž. 2013. Lysiphlebus orientalis (Hymenoptera, Braconidae), a new invasive aphid parasitoid in Europe – evidence from molecular markers. Bull. Entomol. Res. 103 (4): 451–457. CrossrefGoogle Scholar

  • Pike K.S., Starý P., Miller T., Miller R., Allison D., Graf G. & Boydston L. 2000. Ephedrus clavicronis sp.n. (Hymenoptera, Braconidae, Aphidiinae), an aphid parasitoid of the Pacific Northwest, and key to Nearctic Ephedrus. J. Kansas Entomol. Soc. 72 (1): 10–16.Google Scholar

  • Posada D. & Crandall K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14 (9): 817–818. CrossrefGoogle Scholar

  • Rakhshani E., Talebi A.A., Starý P., Tomanović Ž., Manzari S. 2007. Aphid-parasitoid (Hymenoptera, Braconidae, Aphidiinae) associations on willows and poplars in Iran. Acta Zool. Hung. 53 (3): 281–292.Google Scholar

  • Samin N., Ghahari H., Gadallah N.S. & Davidian E. 2014. A study on the Braconidae (Hymenoptera: Ichneumonoidea) from West Azarbaijan province, Northwestern Iran. Linzer Biol. Beitr. 46 (2): 1447–1478.Google Scholar

  • Sanchis A., Latorre A., Gonzalez–Candelas F. & Michelena J.M. 2000. An 18S rDNA-based molecular phylogeny of Aphidiinae (Hymenoptera: Braconidae). Mol. Phylogenet. Evol. 14 (2): 180–194. CrossrefGoogle Scholar

  • Schlinger E.I. & Hall J.C. 1960. Biological notes on Pacific coast aphid parasites, and lists of California parasites (Aphidiinae) and their aphid hosts (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am. 53 (3): 404–15. CrossrefGoogle Scholar

  • Sharkey M.J. & Wharton R.A. 1997. Morphology and terminology, pp. 19–38. In: Wharton R.A., Marsh P.M. & Sharkey M.J. (eds), Manual of the New World Genera of the Family Braconidae. Special Publication of the International Society of Hymenopterists 1, Washington D.C., 439 pp.Google Scholar

  • Shi M. & Chen X.X. 2005. Molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae) based on DNA sequences of 16S rRNA,18S rDNA and ATPase 6 genes. Eur. J. Entomol. 102 (2): 133–138. CrossrefGoogle Scholar

  • Smith M.A., Rodriguez J.J., Whitfield J.B., Deans A.R., Janzen D.H., Hallwachs W. & Hebert P.D. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc. Natl. Acad. Sci. USA 105 (34): 12359–12364. CrossrefGoogle Scholar

  • Starý P. 1962. Notes on the European species of the genus of Ephedrus Haliday (Hymenoptera: Aphidiidae). Opusc. Entomol. 27: 87–98. DOI:10.1163/187631282X00156CrossrefGoogle Scholar

  • Starý P. 1966. Aphid Parasites of Czechoslovakia. Dr. W. Junk Publishers, The Hague, 242 pp. ISBN: 978-94-017-5225-1Google Scholar

  • Starý P. 1967. A review of hymenopterous parasites of citrus pest aphids of the world and biological control projects (Hym., Aphidiidae; Hom., Aphidoidea). Acta Entomol. Bohemoslov. 64: 37–61.Google Scholar

  • Starý P. 1973. A revision of the fossil Aphidiidae (Hymenoptera). Annot. Zool. Bot. 87: 1–22.Google Scholar

  • Starý P.1974. Parasite spectrum (Hym., Aphidiidae) of aphids associated with Galium. Entomol. Scand. 5: 73–80.CrossrefGoogle Scholar

  • Starý P. 1975. Parasites (Hymenoptera, Aphidiidae) of leafcurling apple aphids in Czechoslovakia. Acta Entomol. Bohemoslov. 72: 99–114.Google Scholar

  • Starý P.1976. Aphid Parasites (Hymenoptera, Aphididae) of the Mediterranean Area. Dr. W. Junk Publishers, The Hague, 95 pp.Google Scholar

  • Starý P. 1979. Aphid Parasites (Hymenoptera, Aphididae) of the Central Asian Area. Dr. W. Junk Publishers, The Hague,114 pp.Google Scholar

  • Starý P. 2006. Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae, Aphidiinae). Academia, Praha, 430 pp. ISBN: 8020013849, 9788020013842Google Scholar

  • Starý P., Remaudière G., Gonzalez D. & Shahrokhi S. 2000. A review and host associations of aphid parasitoids (Hym., Braconidae, Aphidiinae) of Iran. Parasitica 56 (1): 15–41.Google Scholar

  • Stelfox A.W. 1941. A list of the Irish species of Toxares and Ephedrus (Hymenoptera: Aphidiidae) with description of these, which include three species new to science. Proc. R. Ir. Acad. B 46 (1940/1941): 125–142.Google Scholar

  • Takada J. 2002. Parasitoids (Hymenoptera: Braconidae, Aphidiinae; Aphelinidae) of four principal pest aphids (Homoptera: Aphididae) on greenhouse vegetable crops in Japan. Appl. Entomol. Zool. 37 (2): 237–249. CrossrefGoogle Scholar

  • 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 (10): 2731–2739. CrossrefGoogle Scholar

  • Tomanović Ž., Kavallieratos N.G., Starý P., Petrović-Obradović O., Tomanović S. & Jovanović S. 2006. Aphids and parasitoids on willows and poplars in southeastern Europe (Homoptera: Aphidoidea; Hymenoptera: Braconidae, Aphidiinae). J. Plant Dis. Protect. 113 (4): 174–180. CrossrefGoogle Scholar

  • Tomanović Ž., Kos K., Petrović A., Starý P., Kavallieratos N.G., Žikić V., Jakse J., Trdan S. & Ivanović 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 (1): 41–47. CrossrefGoogle Scholar

  • Tomanović Z., Petrović A., Kavallieratos N.G., Starý P., Tosevski I.& Mitrovski-Bogdanović A. 2009. Areopraon chaitophori n. sp. (Hymenoptera: Braconidae: Aphidiinae) associated with Chaitophorus leucomelas Koch on poplars, with a key for European Areopraon Mackauer species. Ann. Soc. Entomol. Fr. 45 (2): 187–192. CrossrefGoogle Scholar

  • Tomanović Ž., Petrović A., Starý P., Kavallieratos N.G., Žikić V. & Rakhshani E. 2009. Ephedrus Haliday (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomol. Serb. 14 (1): 39–53.Google Scholar

  • Tomić M., Tomanović Ž., Kavallieratos N.G., Starý P., Athanassiou C.G., Tomić V. & Lučić L. 2005. Morphological variability of several biotypes of Ephedrus plagiator (Nees 1811) (Hymenoptera: Braconidae: Aphidiinae) with the description of a new species. Zool. Anz. 244: 153–162.Google Scholar

  • Yu D.S., van Achterberg C. & Horstman K. 2012. Taxapad 2012, Ichneumonoidea 2011. Database on flash-drive. www.taxapad.com. Ottawa, Ontario, Canada.

  • Žikić V., Stanković S.S., Ilić-MiloševićM., Petrović-Obradović O., Petrović A., Starý P. & Tomanović Ž. 2015. First detection of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiinae) in Serbia; an introduced species invading Europe? N. West. J. Zool. 11 (1): 97–101.Google Scholar

  • Žikić V., Tomanović Z., Ivanović A., Kavallieratos N.G., Starý P., Stanisavljević L. & Rakhshani E. 2009. Morphological characterization of Ephedrus persicae biotypes (Hymenoptera: Braconidae: Aphidiinae) in the Palaearctic. Ann. Entomol. Soc. Am. 102 (1): 1–11. CrossrefGoogle Scholar

  • Žikić V., Tomanović Ž., Kavallieratos N.G., Starý P. & Ivanović A. 2010. Does allometry account for shape variability in Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae) parasitic wasps? Org. Divers. Evol. 10 (5): 373–380. CrossrefGoogle Scholar

About the article

Received: 2016-07-21

Accepted: 2016-11-25

Published Online: 2017-01-11

Published in Print: 2016-12-01

Citation Information: Biologia, Volume 71, Issue 12, Pages 1386–1394, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.1515/biolog-2016-0165.

Export Citation

© 2016 Institute of Zoology, Slovak Academy of Sciences.Get Permission

Comments (0)

Please log in or register to comment.
Log in