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Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae)

Published online by Cambridge University Press:  12 May 2014

Ž. Tomanović ,
A. Petrović ,
M. Mitrović ,
N.G. Kavallieratos ,
P. Starý ,
E. Rakhshani ,
M. Rakhshanipour ,
A. Popović ,
A.H. Shukshuk  and
A. Ivanović
Ž. Tomanović
Affiliation:
Faculty of Biology, Institute of Zoology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
A. Petrović*
Affiliation:
Faculty of Biology, Institute of Zoology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
M. Mitrović
Affiliation:
Department of Plant Pests, Institute for Plant Protection and Environment, Banatska 33, 11080 Zemun, Serbia
N.G. Kavallieratos
Affiliation:
Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 Stefanou Delta str., Kifissia, 14561, Attica, Greece
P. Starý
Affiliation:
Laboratory of Aphidology, Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 37005 České Budějovice, Czech Republic
E. Rakhshani
Affiliation:
Department of Plant Protection, College of Agriculture, Zabol University, P.O.Box: 998615-538, Zabol, I.R. Iran
M. Rakhshanipour
Affiliation:
Faculty of Basic Science, University of Zabol, P.O.Box: 998615-538, Zabol, I.R.Iran
A. Popović
Affiliation:
Faculty of Biology, Institute of Zoology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
A.H. Shukshuk
Affiliation:
Elmergib University Faculty of Arts and Sciences, Zliten, Libya
A. Ivanović
Affiliation:
Faculty of Biology, Institute of Zoology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
*
*Author for correspondence Phone: +381 11 2187 266 Fax: +381 11 2638 500 E-mail: [email protected]
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Abstract

We have identified the following three taxa related to the Aphidius colemani species group, which are important biological control agents: Aphidius colemani, Aphidius transcaspicus and Aphidius platensis. Using partial sequences of the mitochondrial cytochrome oxidase subunit I (mtCOI) gene and geometric morphometric analysis of the forewing shape, we have explored the genetic structure and morphological variability of the A. colemani group from different aphid host/plant associations covering a wide distribution area. The topology of the maximum parsimony and maximum likelihood trees were identical with 98–100% bootstrap support, clustering A. colemani, A. platensis and A. transcaspicus into separate species. The distances among the taxa ranged from 2.2 to 4.7%, which is a common rate for the between-species divergence within the subfamily Aphidiinae. Differences in the shape of the forewing investigated within the biotypes of A. colemani group are congruent with their genetic diversification. Both A. platensis and A. colemani share a common host range pattern, and it would be interesting to estimate and compare the role of these two species in future biological control strategies against aphids of economic importance. Our results indicate that ‘genetic screening’ is a reliable approach for identification within the A. colemani group. The high variation in the wing shape among species, including a significant divergence in the wing shape among specimens that emerged from different hosts, makes the forewing shape and wing venation less reliable for species determination. Aphidius platensis is diagnostified and redescribed, and the key for the A. colemani group is presented.

Keywords

aphid parasitoidsAphidiusmtCOI barcodinggeometric morphometrics
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 5 , October 2014 , pp. 552 - 565
Copyright
Copyright © Cambridge University Press 2014 

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References

Brethes, J. (1913) Himenopteros de la America meridional. Annales Museum National Buenos Aires 24, 35–165.Google Scholar
Clement, M., Posada, D.C. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
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). Molecular Ecology Resources 12, 197–208.CrossRefGoogle ScholarPubMed
Eady, R.D. (1969) A new diagnostic character in Aphidius (Hymenoptera: Braconidae) of special significance in species on pea aphid. Proceedings of the Royal Entomological Society of London 38, 165–173.Google Scholar
Fernandez, C. & Nentwig, W. (1997) Quality control of the parasitoid Aphidius colemani (Hym., Aphidiidae) used for biological control in greenhouses. Journal of Applied Entomology 121, 447–456.CrossRefGoogle 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. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Hågvar, E.B. & Hofsvang, T. (1991) Aphid parasitoids (Hymenoptera, Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information 12, 13–42.Google Scholar
Hasegawa, M., Kishino, H., & Yano, T. (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.CrossRefGoogle ScholarPubMed
Jafari-Ahmadabadi, N.J., Karimi, J., Awal, M.M. & Rakhshani, E. (2011) Morphological and molecular methods in identification of Aphidius transcaspicus Telenga (Hym: Braconidae: Aphidiinae) parasitoid of Hyalopterus spp. (Hom: Aphididae) with additional data on Aphidiinae phylogeny. Journal of the Entomological Research Society 13, 91–103.Google Scholar
Kavallieratos, N.G. & Lykouressis, D. (1999) Redescription of Aphidius transcaspicus Telenga and its distinction from Aphidius colemani Viereck (Hymenoptera Braconidae). Bollettino-Laboratorio di Entomologia Agraria Filippo Silvestri Portici 55, 105–105.Google Scholar
Kavallieratos, N.G., Tomanović, Ž., Starý, P., Athanassiou, C.G., Sarlis, G.P., Petrović, O., Niketić, M. & Veroniki, M.A. (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology 39, 527–563.CrossRefGoogle Scholar
Kavallieratos, N.G., Tomanović, Ž., Starý, P. & Mitrovski-Bogdanović, A. (2008) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Prunoideae and Maloideae crops in Southeast Europe: aphidiine-aphid-plant associations and key. Zootaxa 1793, 47–64.CrossRefGoogle Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.CrossRefGoogle ScholarPubMed
Kos, K., Petrović, A., Starý, P., Kavallieratos, N.G., Ivanović, A., Toševski, I. & Tomanović, Ž. (2011) On the identity of cereal aphid parasitoid wasps Aphidius uzbekistanicus, Aphidius rhopalosiphi, and Aphidius avenaphis (Hymenoptera: Braconidae: Aphidiinae) by examination of COI mitochondrial gene, geometric morphometrics, and morphology. Annals of the Entomological Society of America 104, 1221–1232.CrossRefGoogle Scholar
Latham, D.R. & Mills, N.J. (2012) Host instar preference and functional response of Aphidius transcaspicus, a parasitoid of mealy aphids (Hyalopterus species). BioControl 57, 603–610.CrossRefGoogle Scholar
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2008) Evolutionary significant units in natural enemies: identifying regional populations of Aphidius transcaspicus (Hymenoptera: Braconidae) for use in biological control of mealy plum aphid. Biological Control 46, 532–541.CrossRefGoogle Scholar
Lozier, J.D. & Mills, N.J. (2009 a) Ecological niche models and coalescent analysis of gene flow support recent allopatric isolation of parasitoid wasp populations in the Mediterranean. PloS ONE 4, e5901.CrossRefGoogle ScholarPubMed
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2009 b) Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus. Bulletin of Entomological Research 99, 83–96.CrossRefGoogle Scholar
Meyer, C.P. & Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, 2229–2238.CrossRefGoogle ScholarPubMed
Mitrovski-Bogdanović, A., Petrović, A., Mitrović, M., Ivanović, A., Žikić, V., Starý, P., Vorburger, C. & Tomanović, Ž. (2013) Identification of two cryptic species within the Praon abjectum group (Hymenoptera: Braconidae: Aphidiinae) using molecular markers and geometric morphometrics. Annals of the Entomological Society of America 106, 170–180.CrossRefGoogle Scholar
Nei, M. & Kumar, S. (2000) Molecular Evolution and Phylogenetics. New York, Oxford University Press.CrossRefGoogle Scholar
Pennacchio, F. (1989) The Italian species of the genus Aphidius Nees (Hymenoptera, Braconidae, Aphidiinae). Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’ 46, 75–106.Google Scholar
Petrović, A., Mitrović, M., Starý, P., Petrović-Obradović, O., Žikić, V., Tomanović, Ž. & Vorburger, C. (2013) Lysiphlebus orientalis (Hymenoptera, Braconidae), a new invasive aphid parasitoid in Europe-evidence from molecular markers. Bulletin of Entomological Research 103, 451–457.CrossRefGoogle Scholar
Rakhshani, E., Talebi, A.A., Starý, P., Tomanović, Ž., Kavallieratos, N.G. & Manzari, S. (2008) A review of Aphidius Nees (Hymenoptera: Braconidae: Aphidiinae) in Iran: host associations, distribution and taxonomic notes. Zootaxa 1767, 37–54.CrossRefGoogle Scholar
Remaudière, G. & Remaudière, M. (1997) Catalogue des Aphididae du Monde. Paris, INRA.Google Scholar
Sandrock, C., Schirrmeister, B. & Vorburger, C. (2011) Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC evolutionary biology 11, 348.CrossRefGoogle Scholar
Sharkey, M.J. & Wharton, R.A. (1997) Morphology and terminology. pp. 19–37in Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (Eds) Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication 1. Washington, DC, International Society of Hymenopterists.Google Scholar
Starý, P. (1970) Biology of aphid parasites (Hymenoptera: Aphidiidae) with respect to integrated control. The Hague, Dr. W. Junk, 643 pp.Google Scholar
Starý, P. (1972) Aphidius platensis Brethes, its distribution and host range (Hymenoptera, Aphidiidae). Oriental Insects 6, 359–370.CrossRefGoogle Scholar
Starý, P. (1973) A review of the Aphidius-species (Hymenoptera, Aphidiidae) of Europe. Annotationes Zoologicae et Botanicae, Bratislava 84, 1–85.Google Scholar
Starý, P. (1975) Aphidius colemani Viereck: its taxonomy, distribution and host range (Hymenoptera, Aphidiidae). Acta Entomologica Bohemoslovaca 72, 156–163.Google Scholar
Starý, P. (1988) Aphidiidae. pp. 171–184in Minks, A.K. & Harrewijn, P. (Eds) Aphids, their Biology, Natural Enemies and Control. Amsterdam, Elsevier.Google Scholar
Starý, P. (1995) The Aphidiidae of Chile (Hymenoptera, Ichneumonoidea, Aphidiidae). Deutsche Entomologische Zeitschrift 42, 113–138.CrossRefGoogle Scholar
Starý, P. (2002) Field establishment of Aphidius colemani Vier. (Hym., Braconidae, Aphidiinae) in the Czech Republic. Journal of Applied Entomology 126, 405–408.CrossRefGoogle Scholar
Starý, P., Sampaio, M.V. & Bueno, V.H.P. (2007) Aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their associations related to biological control in Brazil. Revista Brasileira de Entomologia 51, 107–118.CrossRefGoogle Scholar
Takada, H. (1998) A review of the Aphidius colemani (Hymenoptera: Braconidae; Aphidiinae) and closely related species indigenous to Japan. Applied Entomology and Zoology 33, 59–66.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. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tomanović, Ž., Kavallieratos, N.G., Starý, P., Athanassiou, C.G., Žikić, V., Petrović-Obradović, O. & Sarlis, G.P. (2003) Aphidius Nees (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro: tritrophic associations and keys. Acta Entomologica Serbica 8, 15–39.Google Scholar
Wang, X.G. & Messing, R.H. (2006) Potential host range of the newly introduced aphid parasitoid Aphidius transcaspicus (Hymenoptera: Braconidae) in Hawaii. Proceedings of the Hawaiian Entomological Society 38, 81–86.Google Scholar
Zelditch, M.L., Swiderski, D.L. & Sheets, H.D. (2012) Geometric Morphometrics for Biologists: A Primer. San Diego, Elsevier Academic Press.Google Scholar
Žikić, V., Tomanović, Ž., Ivanović, A., Kavallieratos, N.G., Starý, P., Stanisavljević, L.Z., & Rakhshani, E. (2009) Morphological characterization of Ephedrus persicae biotypes (Hymenoptera: Braconidae: Aphidiinae) in the Palaearctic. Annals of the Entomological Society of America 102, 1–11.CrossRefGoogle Scholar