Abstract
Egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) are important natural enemies of many lepidopterous pests in agricultural and forest areas. Because the use of indigenous Trichogramma populations/species can significantly increase the biological control efficiency, the characterization of endemic populations and precise species identification is important. In this study, Trichogramma wasps were collected from parasitized eggs of several lepidopteran pests in Northern and Central Iran. Seven Trichogramma species were identified based on the morphology and the nucleotide sequence, size and restriction profile (PCR-RFLP) of the internal transcribed spacer 2 (ITS2) region of the rDNA of T. brassicae Bezdenko, T. cacoeciae Marchal, T. embryophagum Hartig, T. evanescens Westwood, T. euproctidis Girault, T. pintoi Voegelé and T. tshumakovae Sorokina. This is the first report of T. euproctidis in Iran. Additionally, natural populations were surveyed for the prevalence of Wolbachia. Two populations of T. brassicae were found to be infected by a single Wolbachia strain which was identified by using a multi-locus sequencing approach.
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References
Baldo L, Bartos JD, Werren JH, Bazzocchi C, Casiraghi M, Panelli S (2002) Different rates of nucleotide substitutions in Wolbachia endosymbionts of arthropods and nematodes: arms race or host shifts? Parasitologia 44:179–187
Baldo L, Lo N, Werren JH (2005) Mosaic nature of wsp (Wolbachia surface protein). J Bacteriol 187:5406–5418
Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microb 72(11):7098–7110
Barnay O, Hommay G, Gertz C, Kienlen JC, Schubert G, Marro JD, Pizzol J, Chavigny P (2001) Survey of natural populations of Trichogramma (Hym., Trichogrammatidae) in the vineyards of Alsace (France). J Appl Entomol 125:469–477
Braig HR, Zhou W, Dobson S, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia. J Bacteriol 180:2373–2378
Breedveld KGH, Tanigoshi LK (2007) Seasonal phenology of Enarmonia formosana (Lepidoptera: Tortricidae) and egg parasitism by Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) in Washington State, USA. J Pest Sci 80:15–19
Chang SC, Hu NT, Hsin CY, Sun CN (2001) Characterization of differences between two Trichogramma wasps by molecular markers. Biol Control 21:75–78
Ciociola AI, Zucchi RA, Stouthamer R (2001) Molecular key to seven Brazilian species of Trichogramma (Hymenoptera: Trichogrammatidae) using sequences of the ITS2 region and restriction analysis. Neotrop Entomol 30(2):259–262
Dang XL, Wen SY, He XF, Pang XF (2005) M-PCR: a powerful method for rapid molecular identification of Trichogramma wasps. J Insect Sci 12:77–85
Diehl SR, Bush GL (1984) An evolutionary and applied perspective of insect biotypes. Ann Rev Entomol 29:471–483
Ebrahimi E (1996) The species of Trichogramma Westwood in Iran. (Abstract 20-102). In: Proceeding XX international congress of entomology, Firenze, Italy, p 639
Ebrahimi D, Pintureau B, Shojai M (1998) Morphological and enzymatic study of the genus Trichogramma (Hym. Trichogrammatidae) in Iran. J Appl Entomol Phytophathol 66:122–141
Farrokhi S, Ashouri A, Shirazi J, Allahyari H, Huigens ME (2010) A comparative study on the functional response of Wolbachia-infected and uninfected forms of the parasitoid wasp Trichogramma brassicae. J Insect Sci 10:167
Fursov V (1995) The taxonomic control of Trichogramma production in Ukraine. In: Wajnberg E (ed) Trichogramma and other egg parasitoids. Les Colloques de l’INRA, vol 73, pp 19–21
Girin C, Boulétreau M (1995) Microorganism-associated variation in host infection efficiency in parasitoid wasp Trichogramma bourarachae (Hymenoptera: Trichogrammatidae). Experientia 52:398–401
Gounou S, Chabi-Olaye A, Poehling HM, Schulthess F (2008) Reproductive compatibility of several East and West African Cotesia sesamiae (Hymenoptra: Braconidae) populations and their crosses and backcrosses using Sesamia calamistis (Lepidoptera: Noctuidae) as the host. Biocontrol Sci Techn 18(3):255–266
Hafez MB, Schmitt A, Hassan SA (1999) The side effects of plant extracts and metabolites of Reynoutria sachalinensis (F. Schmidt) Nakai and conventional fungicides on the beneficial organism Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae). J Appl Entomol 123:363–368
Hall TA (1999) BioEdit: A user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hansen LS (2000) Development time and activity threshold of Trichogramma turkestanica on Ephestia kuehniella in relation to temperature. Entomol Exp Appl 96:185–188
Hassan SA (1994) Strategies to select Trichogramma species for use in biological control. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 55–71
Hoffmann AA, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 42–80
Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–948
Hopper KR, Roush RT, Powell W (1993) Management of genetics of biological control introductions. Ann Rev Entomol 38:27–51
Horjus M, Stouthamer R (1995) Does infection with thelytoky causing Wolbachia in pre-adult and adult life stages influence the adult fecundity of Trichogramma deion and Muscidifurax uniraptor? Proc Exp Appl Entomol 6:35–40
Huelsenbeck JP, Roniquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Huigens ME, Stouthamer R (2003) Parthenogenesis associated with Wolbachia. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC Press, Boca Raton, pp 247–266
Huigens ME, Luck RF, Klaassen RHG, Maas MFPM, Timmermans MJTN, Stouthamer R (2000) Infectious parthenogenesis. Nature 405:178–179
Huigens ME, Almedia RP, Boons PAH, Luck RF, Stouthamer R (2004) Natural intraspecific and interspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc R Soc Lond 271:509–515
Hurst GDD, Johnson AP, Schulenburg JH, Fuyama Y (2000) Male killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156:699–709
Jager CR, Pintureau B, Heddi A (1998) Comparison between phylogenetic trees of some Trichogramma species and their Wolbachia endosymbionts. Russ Entomol J 7:163–168
Jeong G, Kim H, Chio Y, Kim W, Park K, Bae S, Kim J, Choi J (2010) Molecular identification of two Trichogramma species (Hymenoptera: Trichogrammatidae) in Korea. J Asia Pac Entomol 13:41–44
Jiggins FM, Hurst GD, Yang Z (2002) Host-symbiont conflicts: positive selection on an outer membrane protein of parasitic but mutualistic Rickettsiaceae. Mol Biol Evol 19:1341–1349
Juchault P, Rigaud GT, Mocquard JP (1992) Evolution of sex determining mechanisms in a wild population of Armadillidium vulgare (Crustacea, Isopoda): competition between two feminizing parasite sex factors. Heredity 69:382–390
Kot J (1964) Experiments in the biology and ecology of species of the genus Trichogramma Westw. and their use in plant protection. Ekol Pol Ser A 12:243–303
Ksentini I, Monje JC, Jardak T, Zeghal N (2010) Naturally occurring egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) in a pomegranate orchard in Tunisia. J Entomol Sci 13:99–106
Kumar GA, Jalali SK, Venkatesan T, Stouthamer R, Niranjana P, Lalitha Y (2009) Internal transcribed spacer-2 restriction fragment length polymorphism (ITS-2-RFLP) tool to differentiate some exotic and indigenous Trichogrammatid egg parasitoids in India. Biol Control 49:207–213
Li YL (1994) Worldwide use of Trichogramma for biological control on different crops: a survey. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB international, Wallingford, pp 37–53
Louis C, Pintureau B, Chapelle L (1993) Recherches sur l’origine de l’unisexualité : la thermothérapie élimine à la fois rickettsies et parthénogenèse thélytoque chez un Trichogramme (Hym., Trichogrammatidae). Comptes Rendus de l’Académie des Sciences de Paris Série III 316:27–33
Luck RF, Stouthamer R, Nunney L (1992) Sex determination and sex ratio patterns in parasitic hymenoptera. In: Wrench DL, Ebbert MA (eds) Evolution and diversity of sex ratio in haplodiploid insect and mites. Chapman and Hall, New York, pp 442–476
Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Cambridge
Nagarkatti S, Nagaraja H (1971) Redescription of some known species of Trichogramma, showing the importance of male genitalia as a diagnostic character. Bull Entomol Res 61:13–31
Nagarkatti S, Nagaraja H (1977) Biosystematics of Trichogramma and Trichogrammatoidea species. Ann Rev Entomol 22:157–176
Neto L, Pintureau B (1995) Taxonomic study of a population of Trichogramma turkestanica discovered in southern Portugal (Hymenoptera: Trichogrammatidae). Ann Soc Entomol Fr 31:21–30
Nylander JAA (2004) Bayesian phylogenetics and the evolution of gall wasps. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1104-232X, p 937
O’Neill SL, Karr T (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178–180
Pinto JD (1999) The systematic of the North American species of Trichogramma. Memoirs Entomol Soc Wash no 22 (1998), p 287
Pinto JD, Stouthamer R (1994) Systematics of the Trichogrammatidae with emphasis on Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 1–36
Pinto JD, Velten RK, Platner GR, Oatman ER (1989) Phenotypic plasticity and characters in Trichogramma. Ann Entomol Soc Am 85:413–422
Pinto JD, Stouthamer R, Platner GR, Oatman ER (1991) Variation in reproductive compatibility in Trichogramma and its taxonomic significance (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 84:37–46
Pinto JD, Kazmer DJ, Planter GR, Sassaman CA (1992) Taxonomy of the Trichogramma minutum complex (Hymenoptra: Trichogrammatidae): allozymic variation and its relationship to reproductive and geographic data. Ann Entomol Soc Am 85:413–422
Pinto JD, Koopmanschap AB, Platner GR, Stouthamer R (2002) The North American Trichogramma (Hymenoptera: Trichogrammatidae) parasitizing certain Tortricidae (Lepidoptera) on apple and pear, with ITS2 DNA characterizations and description of a new species. Biol Control 23:134–142
Pinto JD, Platner GR, Stouthamer R (2003) The systematic of the Trichogramma minutum species complex (Hymenoptera: Trichogrammatidae), a group of important North American biological control agents: the evidence from reproductive compatibility and allozymes. Biol Control 27:167–180
Pintureau B (1997) Systematic and genetical problems revised in two closely related species of Trichogramma, T. embryophagum and T. cacoeciae (Hym., Trichogrammatidae). Miscellania Zoologica 20:11–18
Pintureau B (2008) Les espèces européennes de Trichogrammes. InLibroVeritas, Cergy-Pontoise
Pintureau B, Babault M (1988) Systématique des espèces africaines des genres Trichogramma Westwood et Trichogrammatoidea Girault (Hym. Trichogrammatidae). Les Colloques de l’INRA 43:97–120
Pintureau B, Chapelle L, Delobel B (1999) Effects of repeated thermic and antibiotic treatments on a Trichogramma (Hym., Trichogrammatidae) symbiont. J Appl Entomol 123:473–483
Pintureau B, Chaudier S, Flassabliere CH, Grenier S (2000) Addition of wsp sequences to the Wolbachia phylogeny tree and stability of the classification. J Mol Evol 51:374–377
Pintureau B, Grenier S, Heddi A, Charles H (2002) Biodiversity of Wolbachia and of their effects in Trichogramma (Hymenoptera: Trichogrammatidae). Ann Soc Entomol Fr 38(4):333–338
Pintureau B, Bourarach K, Rohi L (2003) Preliminary inventory of Hymenopteran egg parasitoids from Morocco. Actes Inst Agron Vét Hassan II 23:163–183
Platner JD, Velten RK, Planoutene M, Pinto JD (1999) Slide-mounting techniques for Trichogramma (Trichogrammatidae) and other minute parasitic Hymenoptera. Entomol News 110:56–64
Rohi L, Pintureau B (2003) Reassessment of Trichogramma euproctidis (Girault, 1911) (Hymenoptera: Trichogrammatidae). Russ Entomol 12:373–379
Rosen D (1986) The role of taxonomy in effective biological control programs. Agric Ecosyst Environ 15:121–129
Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc Lond B 250:91–98
Sandrock C, Vorburger C (2011) Single locus recessive inheritance of asexual reproduction in a parasitoid wasp. Curr Biol 21:433–437
Sappal NP, Jeng RS, Hubbes M, Liu F (1995) Restriction fragment length polymorphisms in polymerase chain reaction amplified ribosomal DNAs of three Trichogramma species. Genome 38:419–425
SAS Institute (1996) SAS for Windows, version 6.12. SAS Institute, Cary, NC
Schilthuizen M, Stouthamer R (1997) Horizontal transmission of parthenogenesis inducing microbes in Trichogramma wasps. Proc R Soc Lond B 264:361–366
Shojai M, Tirgari S, Nasrollahi A (1988) Primary report on the occurrence of Trichogramma. In: Trichogramma and other egg parasites. Les Colloques de I’INRA, vol 43, p 121
Silva IMMS, Honda J, van Kan F, Hu J, Neto L, Pintureau B, Stouthamer R (1999) Molecular differentiation of five Trichogramma species occurring in Portugal. Biol Control 16:177–184
Sorokina AP (1984) New species of the genus Trichogramma Westw. (Hymenoptera, Trichogrammatidae) from the USSR. Entomologicheskoe Obozrenie 63(1):154–156
Stouthamer R, Kazmer DJ (1994) Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73:317–327
Stouthamer R, Luck RF (1993) Influence of microbe-associated parthenogenesis on the fecundity of Trichogramma deion and T. pretiosum. Entomol Exp Appl 67:183–192
Stouthamer R, Pinto JD, Platner GR, Luck RF (1990) Taxonomic status of thelytokous forms of Trichogramma. Ann Entomol Soc Am 83:475–481
Stouthamer R, Breeuwer JAJ, Luck RF, Werren JH (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66–68
Stouthamer R, Luko S, Mak F (1994) Influence of parthenogenesis Wolbachia on host fitness. Norw J Agric Sci 16:117–122
Stouthamer R, Breeuwer JAJ, Hurst GDD (1999a) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Ann Rev Microbial 53:71–102
Stouthamer R, Hu J, van Kan FJPM, Platner GR, Pinto JD (1999b) The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma. BioControl 43:421–440
Stouthamer R, Gai Y, Koopmanschap AB, Platner GR, Pinto JD (2000) ITS-2 sequences do not differ for the closely related species Trichogramma minutum and T. platneri. Entomol Exp Appl 95:105–111
Sumer F, Tuncbilek AS, Oztemiz S, Pintureau B, Rugman-Jones P, Stouthamer R (2009) A molecular key to the common species of Trichogramma of the Mediterranean region. BioControl 54:617–624
Taylor MJ, Hoerauf A (1999) Wolbachia bacteria of filarial nematodes. Parasitol Today 15:437–442
Thomson L, Rundle BJ, Carew ME, Hoffmann AA (2003) Identification and characterization of Trichogramma species from south-eastern using the internal transcribed spacer 2 (ITS2) region of the ribosomal gene complex. Entomol Exp Appl 106:235–240
Van Meer MMM, Witteveldt J, Stouthamer R (1999) Phylogeny of arthropod endosymbiont Wolbachia based on wsp gene. Insect Mol Biol 8(3):399–403
Vavre F, Girin C, Boulétreau M (1999) Phylogenetic status of fecundity-enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Mol Biol 8:67–72
Vavre F, De Jong JH, Stouthamer R (2004) Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae. Heredity 93:592–596
Walsh PS, Metzgar DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513
Werren JH (1997) Biology of Wolbachia. Ann Rev Entomol 42:587–609
Werren JH, Bartos JD (2001) Recombination in Wolbachia. Curr Biol 11:431–435
Acknowledgments
We are grateful to Dr. Bernard Pintureau in (INRA/INSA) France for morphological identifying Trichogramma samples. Thijs Machtelinckx is supported by grant number SB-73469 from the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen). Thomas Van Leeuwen is a post-doctoral fellow of the Research Foundation Flanders (FWO).
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Poorjavad, N., Goldansaz, S.H., Machtelinckx, T. et al. Iranian Trichogramma: ITS2 DNA characterization and natural Wolbachia infection. BioControl 57, 361–374 (2012). https://doi.org/10.1007/s10526-011-9397-z
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DOI: https://doi.org/10.1007/s10526-011-9397-z