Molecular and morphological identification of hymenoptran parasitoids from the pomegranate aphid, Aphis punicae in Razavi Khorasan province, Iran

Year 2014, , 291 - 306, 01.06.2014

Hadi Farrokhzadeh Gholamhossein Moravvej Mehdi Modarres Awal Javad Karımı

https://doi.org/10.16970/ted.79294

Cited By: 2

Abstract

Parasitoids play the positive role in aphids control management by keeping the population of aphids below the economic threshold. The pomegranate aphid, Aphis punicae is attacked by several parasitoids which mostly belong to Aphidiinae subfamily. The identification of parasitoids and hyperparasitoids is problematic due to their small size and ambiguous morphological characteristics. The analysis of molecular data of DNA sequences has been suggested as a complementary approach to the classical methods to identify biocontrol agents. In the present study, active parasitoids and hyperparasitoids of the pomegranate aphid collected from Razavi Khorasan province were identified using morphological characters and analysis of two gene sequences including COI and 28S. Phylogenetic analysis was performed using Maximum parsimony and Bayesian methods. The identified parasitoids were Binodoxys angelicae, Lysiphlebus fabarum, Ephedrus persicae, and the hyperparasitoids were Syrphophagus aphidivorus, Alloxysta sp. and Pachyneuron sp. We demonstrated that the mitochondrial COI gene was superior for the identification of these insects compared to the nuclear 28S (D2- region) and that it was compatible with morphological studies. This is the first study on molecular identification of the parasitoids and hyperparasitoids on pomegranate aphids in Iran

Keywords

Pomegranate, parasitoids, COI, 28S, aphids, identification

Razavi Horasan (İran) bölgesinde Nar biti (Aphis punicae)'in hymenopter parazitoitlerinin moleküler ve morfolojik tanılanması

Abstract

Parazitoidler yaprak bitleri populasyonunu ekonomik eşiğin altında tutarak kontrol yönetiminde olumlu bir rol oynar. Nar yaprakbiti, (Aphis punicae) çoğunlukla Aphidiinae alt familyasına ait çeşitli parazitoitler tarafından saldırıya uğramaktadır. Parazitoitleri ve hiperparazitoidlerin tanımlanması, küçük boyutları ve belirsiz morfolojik özellikleri nedeniyle sorunludur. DNA dizilerinin moleküler veri analizi, biyokontrol ajanlarını tanımlamak için klasik yöntemlere tamamlayıcı bir yaklaşım olarak önerilmiştir. Bu çalışmada, Razavi Horasan ilinden toplanan nar yaprak bitinin aktif parazitoitleri ve hiperparazitoidleri morfolojik karakterler kullanılarak ve iki gen dizisinin COI ve 28S’in analizi de dahil olmak üzere tanımlanmıştır. Filogenetik analiz maksimum parsimoni Bayesian yöntemleri kullanılarak gerçekleştirilmiştir. Tanımlanan parazitoidler Binodoxys angelicae, Lysiphlebus fabarum, Ephedrus persicae, hiperparazitoidler Syrphophagus aphidivorus, Alloxysta sp. ve Pachyneuron sp.’dir. Mitokondriyal COI geninin bu böceklerin tanımlanması için Nükleer 28S’e göre (D2 bölge) üstün olduğu ve morfolojik çalışmalar ile uyumlu olduğu tespit edilmiştir. Bu çalışma, İran'da nar yaprakbiti parazitoit ve hiperparazitoidlerinin moleküler tanımlaması açısından ilk çalışmadır

Keywords

Nar, parazitoitler, COI, 28S, afitler, tanılama

References

• Alford, D. V. 2007. Pests of Fruit Crops: A Color Handbook, Academic Press.
• Barahoei, H., E. Rakhshani, E. Nader, P. Starý, N. G. Kavallieratos, Ž. Tomanović & M. Mehrparvar, 2014. Checklist of Aphidiinae parasitoids (Hymenoptera: Braconidae) and their host aphid associations in Iran. Journal of Crop Protection, 3 (2): 199-232.
• Bayhan, E., S. ÖLmez-Bayhan, M. R. Ulusoy & J. K. Brown, 2005. Effect of Temperature on the Biology of Aphis punicae (Passerini) (Homoptera: Aphididae) on Pomegranate. Environmental Entomology, 34 (1): 22-26.
• Belshaw, R. & D. L. J. Quicke, 1997. A molecular phylogeny of the aphidiinae (Hymenoptera: Braconidae). Molecular Phylogenetics and Evolution, 7 (3): 281–293.
• Bigler, F., J. S. Bale, M. J. W. Cock, H. Dreyer, R. Greatrex, U. Kuhlmann, A. J. M. Loomans & J. C. van Lenteren, 2005. Guidelines on information requirements for the import and release of invertebrate biological control agents in European countries. Biocontrol News and Information, 26: 115–123.
• Campbell, B. C., J. D. Steffen-Campbell & J. H. Werren, 1993. Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Molecular Biology, 2 (4): 225–237.
• Carver, M., 1989. Biological control of Aphids. Natural Enemies and Control, 2: 171–184.
• Compere, H., 1961. The red scale and its insect enemies. Hilgardia, 31: 173–278.
• Crozier, R. H., Y. C. Crozier & A. G. Mackinlay, 1989. The COI and COII region of honeybee mithochondrial DNA: evidence for variation in insect mitochondrial evolutionary rates. Molecular Biology and Evolution, 6: 399-411.
• Darsouei, R., J. Karimi & M. Modarres-Awal, 2011. Parasitic wasps as natural enemies of aphid populations in the Mashhad region of Iran: new data from DNA barcodes and SEM. Archives of Biological Science Belgrade, 63 (4): 1225-1234.
• Derocles, S. A. P., A. l. Ralec, M. Plantegenest, B. Chaubet, C. Cruaud, A. Cruaud & J. Y. Rasplus, 2011. Identification of molecular markers for DNA barcoding in the Aphidiinae (Hymenoptra: Braconidae). Molecular Ecology Resources, 12 (2): 197-208.
• Dowton, M. & A. D. Austin, 1997. Evidance for AT tranversion bias in wasp (Hymenoptra: Symphyta) mitochondrial genes and its implications for the origin of parasitism. Journal of Molecular Evolution, 44 (4): 398-405.
• Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39 (4): 783-791.
• Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5): 294-299.
• Fre´zal, L. & R. Leblois, 2008. Four years of DNA barcoding: current advances and prospects. Infection, Genetics and Evolution, 8: 727–736.
• Gibson, G. A. P., 1985. some pro and mesothoratic structures important for phylogenetic analysis of hymenoptera, with review of terms used for the structures. The Canadian Entomologist, 117 (11): 1395-1443.
• Gimeno, C., R. Belshaw & D. L. J. Quicke, 1997. phylogenetic relationship of Alysiinae/Opiinae (Hymenoptera: braconidae) and the utility of cytochorom b, 16S and 28S D2 rRNA. Insect Molecular Biology, 6 (3): 273-284.
• Gotelli, N., 2004. A taxonomic wish-list for community ecology. Philosophical Transactions of the Royal Society of London (B), 359: 585–597.
• Hall, T., 1999. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
• Hancock, J. M., D. Tautz & G. A. Dover, 1988. Evolution of the secondary structure and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. Molecular Biology and Evolution, 5 (4): 393–414.
• Hillis, D. M., C. Moritz & B. K. Mable 1996. Molecular Systematic, Sunderland, Massachusetts U.S.A.
• Huelsenbeck, J. P. & F. Ronquist, 2001. MrBayes: bayesian inference of phylogenetic trees. Bioinformatics, 17: 754– 755.
• Karimi, J., R. Darsouei, S. Fathah-Hosseini & H. Sadeghi, 2012. Phylogenetic analysis on some Iranian white grubs with new data about natural pathogen of Polyphylla adspersa. Journal of the Entomological Research Society, 14 (1): 01-13.
• Kavallieratos, N. G., D. P. Lykouressis, G. P. Sarlis, G. J. Stathas, A. S. Segovia & C. G. thanassiou, 2001. The Aphidiinae (Hymenoptera: Ichneumonoidea:Braconidae) of Greece. Phytoparasitica, 29 (4): 306–340.
• Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2): 111-120.
• Linares, A. R., J. M. Hancock & G. A. Dover, 1991. Secondary structure constraints on the evolution of Drosophila 28S ribosomal RNA expansion segments. Molecular Biology and Evolution, 219 (4): 381–390.
• Linares, M. C., N. I. Soto-Caldero, D. Lees & N. M. Anthony, 2009. High mitochondrial diversity in geographically widespread butterflies of Madagascar: a test of the DNA barcoding approach. Molecular Phylogenetics and Evolution, 50: 485-495.
• Linnen, C. R. & B. Farrell, 2008. Phylogenetic analysis of nuclear and mitochondrial genes reveals evolutionary relationships and mitochondrial introgression in the sertifer species group of the genus Neodiprion (Hymenoptera : Diprionidae). Molecular Phylogenetics and Evolution, 48: 240-257.
• Mackauer, M. & P. Starý 1967. World Aphidiidae (Hymenoptera: Ichneumonoidea), Le Francois, Paris.
• Meier, R., K. Shiyang, G. Vaidya & P. K. L. Ng, 2006. DNA barcoding and taxonomy in Diptera: A tale of high intraspecific variability and low identification success. Systematic Biology, 55 (5): 715-728.
• Moawad, S. S. & A. M. F. Al-Barty, 2011. Evaluation of some medicinal and ornamental plant extracts toward pomegranate aphid, Aphis punicae (Passerini) under laboratory conditions. African Journal of Agricultural Research, 6 (10): 2425-2429.
• Murat, A. M., N. Uygun & P. Starý, 2004. A survey of aphid parasitoids in Kahramanmaras, Turkey (Hymenoptera: Braconidae, Aphidiinae; and Hymenoptera: Aphelinidae). Phytoparasitica, 32 (3): 255-263.
• Nazari, Y., A. A. Zamani, S. M. Masoumi, E. Rakhshani, O. Petrović-Obradović, S. Tomanović, P. Starý & Ž. Tomanović, 2012. Diversity and host associations of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in the farmlands of western Iran. Acta Entomologica Musei Nationalis Pragae, 52: 559-584.
• Pederson, B. V., 1996. A phylogenetic analysis of cuckoo bumble-bee (Psythyrus, Lepeletier) and bumblebees (Bombus, Latreille) inferred from sequences of the mitochondrial gene cytochrom oxidase I. Molecular Phylogenetics and Evolution, 5 (2): 289-297.
• Rakhshani, E., S. Kazemzadeh, P. Starý, H. Barahoei, N. G. Kavallieratos, A. Ćetković, A. Popović, I. Bodlah & Ž. Tomanović, 2012. Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northeastern Iran: Aphidiine-aphid- plant associations, key and description of a new species. Journal of Insect Science, 12 (143): 1-26.
• Rakhshani, E., Ž. Tomanović, P. Starý, N. G. Kavallieratos, M. Ilić, S. S. Stanković & M. N. Rajabi, 2011. Aphidiinae parasitoids (Hymenoptera: Braconidae) of Macrosiphoniella aphids (Hemiptera: Aphididae) in the western Palaearctic region. Journal of Natural History, 45 (41): 2559–2575.
• Rosen, D. & P. Debach, 1973. Systematics, morphology and biological control. BioControl, 18: 215–222.
• Rouhani, M., M. A. Samih, H. Izadi & E. Mohammadi, 2013. Toxicity of new insecticides against pomegranate aphid, Aphis punicae. International Research Journal of Applied and Basic Sciences, 4 (3): 496-501.
• Sanchis, A., A. Latorre, F. Gonzalez-Candelas, J. Michelena & M. Mackauer, 2000. An 18S rDNA-based molecular phylogeny of Aphidiinae (Hymenoptera: Braconidae). Molecular Phylogenetics and Evolution, 14 (2): 180–194.
• Sayed, S. M., M. M. Montaser, G. Elsayed & S. A. M. Amer, 2013. Preliminary molecular identification of a predatory bug, Orius albidipennis, collected from ornamental plants. Journal of Insect Science, 13: 1-11.
• Sha, Z. L., C. D. Zhu, R. W. Murphy & D. W. Huang, 2007. Diglyphus isaea (Hymenoptera: Eulophidae): a probable complex of cryptic species that forms an important biological control agent of agromyzid leaf miners. Journal of Zoological Systematics and Evolutionary Research, 45: 128-135.
• Shi, M. & X.-X. Chen, 2005. Molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae) based on DNA sequences of 16S rRNA, 18S rDNA and ATPase 6 genes. European Journal of Entomology, 102 (2): 133– 138.
• Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu & P. Flook, 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymeras chain reaction primers. Annal Entomological Society of Amercia, 87 (6): 1-51.
• Smith, P., S. Kambhampati, W. Volkl & M. Mackauer, 1999. A phylogeny of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) inferred from mitochondrial NADH 1 dehydrogenase gene sequence. Molecular Phylogenetics and Evolution, 11 (2): 236–245.
• Starý, P., 1970. Biology of Aphid Parasites (Hymenoptera: Aphidiidae) with Respect to Integrated Control. Series Entomologica (The Hague), 6: 643.
• Starý, P., 1973. A review of the Aphidius-species (Hymenoptera, Aphidiidae) of Europe. Annotationes Zoologicae et Botanicae, 84: 58.
• Starý, P., 1988. Aphidiidae. In Aphids, their Biology. Natural Enemies and Control, 2: 171–184.
• Starý, P. & J. Havelka, 2008. Fauna and association of aphid parasitoids in an up-dated farmland area. Bulletin of Insectology, 61 (2): 251-276.
• Starý, P., E. Rakhshani, J. Havelka, Ž. Tomanović, N. G. Kavallieratos & M. Sharkey, 2010. Review and Key to the World Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Greenideinae Aphids (Hemiptera: Aphididae), Including Notes on Invasive Pest Species. Annals of the Entomological Society of America, 103 (3): 307-321.
• Swofford, D. L. 2002. PAUP*: Phylogenetic Analysis using Parsimony. Version 4.0b. Sunderland, MA, Sinauer Associates.
• Talebi, A. A., E. Rakhshani, Y. Fathipour, P. Starý, ŽeljkoTomanoviæ & N. Rajabi-Mazhar, 2009. Aphids and their parasitoids (Hym., Braconidae: Aphidiinae) associated with medicinal plants in Iran. American-Eurasian Journal of Sustainable Agriculture, 3 (2): 205-219.
• Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28 (10): 2731-2739.
• Tomanovic, Z. & N. G. Kavallieratos, 2002. Trioxys Haliday (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro. Acta entomologica serbica, 7 (2): 67–81.
• Tomanovic, Z., N. G. Kavallieratos & P. Starý, 2003. Aphidius Nees aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica, 8: 15–39.
• Traugott, M., J. R. Bell, G. R. Broad, W. Powell, F. J. F. Vanveen, I. M. G. Vollhardt & W. O. C. Symondson, 2008. Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Molecular Ecology, 17 (17): 3928–3938.
• Valentini, A., F. Pompanon & P. Taberlet, 2009. Barcoding for ecologist. Trends in Ecology and Evolution, 24: 110– 117.
• Zhou, Q.-S., Y.-Q. Xi, F. Yu, X. Zhang, X.-J. Li, C.-L. Liu, Z.-Q. Niu, C.-D. Zhu, G.-X. Qiao & Y.-Z. Zhang, 2014. Application of DNA barcoding to the identification of Hymenoptera parasitoids from the soybean aphid (Aphis glycines) in China. Insect Science, 21 (3): 363-373.
• Zumoffen, L., A. Salvo, C. E. Salto, R. G. Manfrino & K. S. Pike, 2013. First record and redescription of Binodoxys brevicornis (Hymenoptera: Braconidae: Aphidiinae) from Argentina. Revista de la Sociedad Entomológica Argentina, 72 (1-2): 91-97.