Abstract
Karyotypes of six species belonging to three main clades of parasitoid Hymenoptera, the superfamilies Ichneumonoidea (Ichneumonidae: Ichneumon amphibolus), Cynipoidea (Cynipidae: Diplolepis rosae) and Chalcidoidea (Eurytomidae: Eurytoma robusta, Eu. serratulae and Eu. compressa, and Torymidae: Torymus bedeguaris) were studied using FISH with 18S rDNA and telomeric (TTAGG)n probes. Haploid karyotypes of D. rosae, Eu. robusta and Eu. serratulae carried the only 18S rDNA hybridization signal, whereas those of I. amphibolus and Eu. compressa carried three and two rDNA clusters respectively. In addition, three rDNA sites were visualized in the aneuploid female of T. bedeguaris. The number of rDNA clusters in parasitoid Hymenoptera generally correlates to the chromosome number. Apart from the overwhelming majority of the studied species of aculeate Hymenoptera, no hybridization signals were obtained from FISH with the telomeric (TTAGG)n probe in the examined parasitoid species. These data suggest absence of the canonical (TTAGG)n insect telomeric motif in the Ichneumonoidea, Cynipoidea and Chalcidoidea, and perhaps in parasitoid Hymenoptera in general.
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References
Belle E, Beckage N, Rousselet J, Poirié M, Lemeunier M, Drezen J-M (2002) Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J Virol 76:5793–5796
Bolsheva NL, Gokhman VE, Muravenko OV, Gumovsky AV, Zelenin AV (2012) Comparative cytogenetic study on two species of the genus Entedon Dalman, 1820 (Hymenoptera: Eulophidae) using DNA-binding fluorochromes and molecular and immunofluorescent markers. Comp Cytogenet 6(1):79–92. doi:10.3897/compcytogen.v6i1.2349
Cabrero J, Camacho JPM (2008) Location and expression of ribosomal RNA genes in grasshoppers: abundance of silent and cryptic loci. Chromosome Res 16:595–607. doi:10.1007/s10577-008-1214-x
Carabajal Paladino L, Papeschi A, Lanzavecchia S, Cladera J, Bressa MJ (2013) Cytogenetic characterization of Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid wasp used as a biological control agent. Eur J Entomol 110(3):401–409. doi:10.14411/eje.2013.054
Chirino MG, Papeschi AG, Bressa MJ (2013) The significance of cytogenetics for the study of karyotype evolution and taxonomy of water bugs (Heteroptera, Belostomatidae) native to Argentina. Comp Cytogenet 7(2):111–129. doi:10.3897/compcytogen.v7i2.4462
Frydrychová R, Marec F (2002) Repeated loss of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115:179–187. doi:10.1023/a:1020175912128
Frydrychová R, Grossmann P, Trubač P, Vítková M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178. doi:10.1139/g03-100
Gokhman VE (2009) Karyotypes of parasitic Hymenoptera. Springer Science + Business Media B.V., Dordrecht, xiii + 183 pp. doi:10.1007/978-1-4020-9807-9
Gokhman VE (2011) Morphotypes of chromosome sets and pathways of karyotype evolution of parasitic Hymenoptera. Russ Entomol J 20(3):265–271. http://zmmu.msu.ru/files/images/spec/Russ%20Ent%20J/ent20_3%20265_271%20Gokhman.pdf
Gokhman VE, Mikhailenko AP (2007) Chromosomes of Torymus bedeguaris (Linnaeus, 1758) and T. chloromerus (Walker, 1833) (Hymenoptera: Torymidae). Russ Entomol J 16(4):471–472
Gokhman VE, Mikhailenko AP (2008) Karyotypic diversity in the subfamily Eurytominae (Hymenoptera: Eurytomidae). Folia biol (Kraków) 56(3–4):209–212. doi:10.3409/fb.56_3-4.209-212
Grozeva S, Kuznetsova VG, Anokhin BA (2011) Karyotypes, male meiosis and comparative FISH mapping of 18S ribosomal DNA and telomeric (TTAGG)n repeat in eight species of true bugs (Hemiptera, Heteroptera). Comp Cytogenet 5(4):335–374. doi:10.3897/compcytogen.v5i4.2307
Heraty J (2009) Parasitoid biodiversity and insect pest management. Chapter 19. In: Foottit RG, Adler PH (eds) Insect biodiversity: science and society. Wiley-Blackwell, UK, pp 445–462. doi:10.1002/9781444308211.ch19
Heraty J, Ronquist F, Carpenter JM, Hawks D, Schulmeister S, Dowling AP, Murray D, Munro J, Wheeler WC, Schiff N, Sharkey M (2011) Evolution of the hymenopteran megaradiation. Mol Phylogenetics Evol 60:73–88. doi:10.1016/j.ympev.2011.04.003
Heraty JM, Burks RA, Cruaud A, Gibson GAP, Liljeblad J, Munro J, Rasplus J-Y, Delvare G, Janšta P, Gumovsky A, Huber J, Woolley JB, Krogmann L, Heydon S, Polaszek A, Schmidt S, Darling DC, Gates MV, Mottern J, Murray E, Molin AD, Triapitsyn S, Baur H, Pinto JD, van Noort C, George J, Yoder M (2013) A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics 29:466–542. doi:10.1111/cla.12006
Hirai H, Yamamoto MT, Ogura K, Satta Y, Yamada M, Taylor RW, Imai HT (1994) Multiplication of 28S rDNA and NOR activity in chromosome evolution among ants of the Myrmecia pilosula species complex. Chromosoma 103(3):171–178. doi:10.1007/bf00368009
Imai HT, Taylor RW, Crosland MWJ, Crozier RH (1988) Modes of spontaneous chromosomal mutation and karyotype evolution in ants with reference to the minimum interaction hypothesis. Jpn J Genet 63:159–185
Kuznetsova VG, Grozeva SM, Anokhin BA (2012) The first finding of (TTAGG)n telomeric repeat in chromosomes of true bugs (Heteroptera, Belostomatidae). Comp Cytogenet 6(4):341–346. doi:10.3897/compcytogen.v6i4.4058
Lorite P, Carillo JA, Palomeque T (2002) Conservation of (TTAGG)n telomeric sequences among ants (Hymenoptera, Formicidae). J Hered 93(4):282–285
Lukhtanov VA, Kuznetsova VG (2010) What genes and chromosomes say about the origin and evolution of insects and other arthropods. Russ J Genet 46:1115–1121. doi:10.1134/s1022795410090279
Maryańska-Nadachowska A, Kuznetsova VG, Karamysheva TV (2013) Chromosomal location of rDNA clusters and TTAGG telomeric repeats in eight species of the spittlebug genus Philaenus (Hemiptera: Auchenorrhyncha: Aphrophoridae). Eur J Entomol 110(3):411–418. doi:10.14411/eje.2013.055
Menezes RST, Silva TM, Carvalho AT, Andrade-Souza V, Silva JG, Costa MA (2013) Numerical and structural chromosome variation in the swarm-founding wasp Metapolybia decorata Gribodo 1896 (Hymenoptera, Vespidae). Genetica 141(7–9):273–280. doi:10.1007/s10709-013-9726-5
Meyne J, Hirai H, Imai HT (1995) FISH analysis of the telomere sequences of bulldog ants (Myrmecia: Formicidae). Chromosoma 104(1):14–18. doi:10.1007/bf00352221
Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, London
Rasnitsyn AP (1980) Origin and evolution of hymenopterous insects. Trudy Paleontologicheskogo Instituta AN SSSR 174. Nauka, Moscow (in Russian)
Schwarzacher T, Heslop-Harrison P (2000) Practical in situ hybridization. BIOS Scientific Publishers Ltd, Oxford, xii + 203 pp
Sharkey MJ (2007) Phylogeny and classification of Hymenoptera. Zootaxa 1668:521–548. http://www.mapress.com/zootaxa/2007f/zt01668p548.pdf
Stille B, Dävring L (1980) Meiosis and reproductive strategy in the parthenogenetic gall wasp Diplolepis rosae (L.) (Hymenoptera, Cynipidae). Hereditas 92:353–362
The Nasonia Genome Working Group (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327(5963):343–348. Supporting online material. http://www.sciencemag.org/content/suppl/2010/01/14/327.5963.343.DC1/Werren.SOM.pdf. Accessed 28 Apr 2014
Van Vugt JJFA, de Nooijer S, Stouthamer R, de Jong H (2005) NOR activity and repeat sequences of the paternal sex ratio chromosome of the parasitoid wasp Trichogramma kaykai. Chromosoma 114:410–419. doi:10.1007/s00412-005-0026-4
Van Vugt JJFA, de Jong H, Stouthamer R (2009) The origin of a selfish B chromosome triggering paternal sex ratio in the parasitoid wasp Trichogramma kaykai. Proc R Soc B 276:4149–4154. doi:10.1098/rspb.2009.1238
Vítková M, Král J, Traut W, Zrzavý J, Marec F (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13:145–156. doi:10.1007/s10577-005-7721-0
Acknowledgments
The present study was partly supported by the research Grant No. 14-04-01051 from the Russian Foundation for Basic Research (RFBR) and programs of the Presidium of the Russian Academy of Sciences “Gene Pools and Genetic Diversity” and “Origin of the Biosphere and Evolution of Geo-Biological Systems”. Dr. Robert B. Angus (School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK) has kindly checked the language of the manuscript.
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Gokhman, V.E., Anokhin, B.A. & Kuznetsova, V.G. Distribution of 18S rDNA sites and absence of the canonical TTAGG insect telomeric repeat in parasitoid Hymenoptera. Genetica 142, 317–322 (2014). https://doi.org/10.1007/s10709-014-9776-3
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DOI: https://doi.org/10.1007/s10709-014-9776-3