Eur. J. Entomol. 106 (1): 1-9, 2009 | 10.14411/eje.2009.001

Chromosomal differentiation among bisexual European species of Saga (Orthoptera: Tettigoniidae: Saginae) detected by both classical and molecular methods

Elżbieta WARCHAŁOWSKA-ŚLIWA1, Beata GRZYWACZ1, Anna MARYAŃSKA-NADACHOWSKA1, Tatjana V. KARAMYSHEVA2, Nikolai B. RUBTSOV2, Dragan P. CHOBANOV3
1 Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland; e-mail: warchalowska@isez.pan.krakow.pl
2 Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia
3 Institute of Zoology, Bulgarian Academy of Sciences, Tsar Osvoboditel 1, 1000 Sofia, Bulgaria

We report the karyotype characteristics including chromosome numbers of Saga campbelli campbelli, S. c. gracilis, and S. rammei using the following classical cytogenetic methods: C-banding, silver staining, and fluorochrome staining DAPI and CMA3. We also present FISH data showing the distribution of telomeric repeats and 18S rDNA on the chromosomes of these species and the results of similar studies cited in the literature on S. hellenica, S. natoliae, and S. rhodiensis. The five European Saga species exhibit a high rate of karyotype evolution. In addition to changes in chromosome number and morphology (by chromosomal inversion and/or chromosome fusion), interspecific autosomal differentiation involved changes in the distribution and quantity of constitutive heterochromatin and GC-rich regions, as well as the number and location of NORs. In the present study we focused on testing a hypothetical model of karyotype evolution in Saga, with particular reference to the cytogenetic mapping of rDNA and telomeric sequences. Variation in the distribution of rDNA and location of Ag-NORs are novel phylogenetic markers for the genus Saga.

Keywords: Orthoptera, Saginae, Saga, karyotype, Ag-NOR, FISH, chromosome, rDNA, telomeric repeats

Received: July 4, 2008; Accepted: September 1, 2008; Published: March 10, 2009

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References

  1. BRIDLE J.R., DE LA TORRE J., BELLA J.L., BUTLIN R.K. & GOSALVEZ J. 2002: Low level of chromosomal differentation between the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera; Acrididae) in northen Spain. Genetica 114: 121-127 Go to original source...
  2. CABRERO J., BUGROV A., WARCHALOWSKA-SLIWA E., LOPEZ-LEON M.D., PERFECTTI F. & CAMACHO J.PM. 2003: Comparative FISH analysis in five species of Eyprepocnemidine grasshoppers. Heredity 90: 377-381 Go to original source...
  3. CABRERO J. & CAMACHO J.P.M. 1986: Cytogenetics studies in gomphocerine grasshopper. I. Comparative analysis of chromosome C-banding pattern. Heredity 56: 365-372 Go to original source...
  4. CABRERO J. & CAMACHO J.P.M. 2008: Location and expresion of ribosomal RNA genes in grasshoppers: Abundance of silent and cryptic loci. Chromosome Res. 16: 595-607 Go to original source...
  5. CABRERO J., GOMEZ R. & CAMACHO J.P.M. 2007: No evidence of the presence of Wolbachia in the parthenogenetic insect Saga pedo. Proc. XI. Eur. Soc. Evol. Biol. Congress, Uppsala, Sweden, 20-25 August 2007. Uppsala, p. 277
  6. CAMACHO J.PM., PASCUAL F., BELDA J. & CABRERO J. 1987: Cytological markers for analyzing evolutionary relationship between related species of orthopteroids. In Baccetti B. (ed.): Evolutionary Biology of Orthopteroid Insects. Ellis Horwood, Chichester, pp. 148-156
  7. CIPLAK B. 2004: Biogeography of Anatolia: the marker group Orthoptera. Mem. Soc. Entomol. Ital. 82: 357-372
  8. COLOMBA M., VITTURI R., VOLPE N., LANNINO A. & ZUNINO M. 2004: Karyotype, banding and rDNA FISH in the scarab beetle Anoplotrupes stercorosus (Coleoptera: Scarabaeoidae: Geotrupidae. Description and comparative analysis. Micron 35: 717-720 Go to original source...
  9. EADES D.C., OTTE D. & NASKRECKI P. 2007: Orthoptera Species File Online. Version 2.0/3.0 http://Orthoptera.SpeciesFile.org (10/05/2007)
  10. FRYDRYCHOVA R. & MAREC F. 2002: Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115: 179-187 Go to original source...
  11. FRYDRYCHOVA R., GROSSMANN P., TRUBAC P, VITKOVA M. & MAREC F. 2004: Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47: 163-178 Go to original source...
  12. GALIAN J., RUA P., SERRANO J., JUAN C. & HEWITT G.M. 1999: Phylogenetic relationship in the west Mediterranean Scartina (Coleoptera: Carabidae) inferred from mitochondrial COI sequence and karyotype analysis. J. Zool. Syst. Evol. Res. 37: 85-92 Go to original source...
  13. GOLDSCHMIDT E. 1946: Poliploidy and parthenogenesis in the genus Saga. Nature 158: 587-588 Go to original source...
  14. GOROCHOV A. 1995: System and Evolution of the Suborder Ensifera (Orthoptera). Part II. Proceedings of the Zoological Institute 260. Russian Academy of Sciences, St. Petersburg, 223 pp
  15. HARZ K. 1969: Die Orthopteren Europas I. Series Entomol 5. Dr W Junk, The Hague, 776 pp
  16. HELLER K.-G. 1988: Bioakustik der europaeischen Laubheuschreken. Josef Margraf, Weikersheim, 358 pp
  17. HEWITT G.M. 1979: Grasshoppers and Crickets. Animal Cytogenetics, 3. Insecta I. Orthoptera. Borntraeger, Berlin, Stuttgart, 170 pp
  18. KALTENBACH A. 1967: Unterlagen fuer eine Monographie der Saginae I. Superrevision der Gattung Saga Charpentier (Saltatoria: Tettigoniidae). Beitr. Entomol. 17: 3-107
  19. KOJIMA K.K., KUBO Y. & FUJIWARA H. 2002: Complex and tandem repeat structure of subtelomeric regions in the Taiwan cricket, Teleogryllus taiwanemma. J. Mol. Evol. 54: 474-485 Go to original source...
  20. KOLICS B., ORCI K.M., CHOBANOV D., BASKA F., KONDOROSY E. & MULLER T. 2008: Description of the song of the bushcricket Saga rammei Kaltenbach, 1965 (Orthoptera: Tettigoniidae). Biologia (Zool.) 63: 1-7 Go to original source...
  21. LA GRECA M. 1999: Il contributo degli Ortotteri (Insecta) alla conoscenza della biogeografia dell'Anatolia: la componente gondwaniana. Biogeographia 20: 179-200
  22. LEMONNIER-DARCEMONT M., DUTRILLAUX A.M., DUTRILLAUX B. & DARCEMONT C. 2008: Recherches sur la phylogenie du genre Saga (Orthoptera: Tettigoniidae) donnees chromosomiques. Ann. Soc. Entomol. Fr. 44 : 477-485 Go to original source...
  23. LEVAN A., FREDGA K. & SANDBERG A.A. 1964: Nomenclature for centromeric position of chromosomes. Hereditas 52: 201-220 Go to original source...
  24. LICHTER P., CREMER T., TANG C.J., WATKINS P.C., MANUELIDIS L. & WARD D.C. 1988: Rapid detection of human chromosome 21 aberration by in situ hybridisation. Proc. Natl. Acad. Sci. USA 85: 9664-9668 Go to original source...
  25. LOPEZ-FERNANDEZ C., PRADILLO E., ZABAL-AGUIRRE M., FERNANDEZ J.L., GARCIA DE LA VEGA C. & GISALVEZ J. 2004: Telomeric and interstitial telomeric-like DNA sequence in Orthoptera genomes. Genome 47: 757-763 Go to original source...
  26. LOPEZ-LEON M.D., CABRERO J. & CAMACHO J.P.M. 1999: Unusually high amount of inactive ribosomal DNA in the grasshopper Stauroderis scalaris. Chromosome Res. 7: 83-88 Go to original source...
  27. LORETO V., CABRERO J., LOPEZ-LEON M.D., CAMACHO J.P.M. & SOUZA M.J. 2008: Comparative analysis of rDNA location in five Neotropical gomphocerine grasshopper species. Genetica 132: 95-101 Go to original source...
  28. MALYGIN A.A., GRAIFER D.M., ZENKOVA M.A., MAMAEV S.V. & KARPOVA G.G. 1992: Affinity modification of 80S ribosomes from human placenta by derivatives of tri- and hexauridylates as mRNA analogs. Mol. Biol. (Moscow) 26: 142-149.
  29. MATTHEY R. 1939: La formule chromosomiale de la sauterelle parthenogenetique Saga serrata Fabr. et de l'Ephippigera vitium. C. R. Soc. Biol. Paris 132: 369-370
  30. MATTHEY R. 1941: Etude biologique et cytologique de Saga pedo Pallas (Orthoptera - Tettigoniidae). Rev. Suisse Zool. 48: 91-102
  31. MATTHEY R. 1946: Demonstration du caractere geographique de la parthenogenese de Saga pedo Pallas et de la polyploidie, par comparaison avec les especes bisexueles S. ephippigera Fisch. et S. gracilipes Uvar. Experientia 2: 260-261 Go to original source...
  32. MATTHEY R. 1948: A propos de la polyploidie de Saga pedo Pallas (Orthoptera - Tettigoniidae). Experientia 4: 26-27 Go to original source...
  33. MATTHEY R. 1949: Les chromosomes de Saga cappadocica Werner (Orthoptera, Tettigoniidae). Arch. J. Klaus Stift. Vererbf. 25: 44-46
  34. MARTINEZ-NAVARRO E.M., SERRANO J. & GALIAN J. 2004: Chromosome evolution in ground beetles: localization of the rDNA loci in the tribe Harpalini (Coleoptera, Carabidae). J. Zool. Dyst. Evol. Res. 42: 38-43 Go to original source...
  35. NATH J. & JOHNSON K.L. 2000: A review of fluorescence in situ hybridization (FISH): current status and future prospects. Biotechn. Histochem. 75: 54-78 Go to original source...
  36. OKAZAKI S., TSUCHIDA K., MAEKAWA H., ISHIKAWA H. & FUJIWARA H. 1993: Identification of a pentanucleotide telomeric sequence, (TTAGG)n in the silkworm Bombyx mori and in other insects. Mol. Cell. Biol. 13: 1424-1432 Go to original source...
  37. ROCHA M.F., SOUZA M.J. & MOURA R.C. 2004: Karyotyic analysis, contitutive heterochromatin and NOR distribution in five grasshopper species of the subfamily Leptysminae (Acrididae). Caryologia 57: 107-116 Go to original source...
  38. SAHARA K., MAREC F. & TRAUT W. 1999: TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 7: 449-460 Go to original source...
  39. SCHNEIDER M.C., ALMEIDA M.C., ROSA S.P., COSTA C. & CELLA D.M. 2006: Evolutionary chromosomal differentiation among four species of Conoderus Eschschltz, 1829 (Coleoptera, Elateridae, Agrypninae, Conoderini) detected by standard staining, C-banding, silver nitrate impregnation, and CMA3/DA/DAPI staining. Genetica 128: 333-346 Go to original source...
  40. SCHWARZACHER T. 2003: DNA, chromosomes, and in-situ hybridization. Genome 46: 953-962 Go to original source...
  41. SCHWEIZER D. 1976: Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58: 307-324 Go to original source...
  42. SOUZA M.J. & HAVER P.R.O. & MELO N.F 2003: Karyotype, C-and fluorochrome banding patterns, NOR location and FISH in the grasshoppers Xestotrachelus robustus (Romelidae). Caryologia 56: 261-267 Go to original source...
  43. SUMNER S.G. 1972: A simple technique for demonstrating centromere heterochromatin. Exp. Cell. Res .75: 304-306 Go to original source...
  44. VITKOVA M., TRAUT W.T., ZRZAVY J. & MAREC F. 2005: The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res. 13: 145-156 Go to original source...
  45. VITTURI R., COLOMBA M.S., BARBIER R. & ZUNINO M. 1999: Ribosomal DNA location in the scarab beetle Thorectes intermedius (Costa) (Coleoptera: Geotruidae) using banding and fluorescent in situ hybridization. Chromosome Res. 7: 255-260 Go to original source...
  46. VITTURI R., COLOMBA M., VOLPE N., LANNINO A. & ZUNINO M. 2003: Evidence for male X0 sex-chromosome system in Pentodon bidens punctatum (Coleoptera: Scarabaeoidea: Scarabaeidae) with X-linked 18S-28SrDNA cluster. Genes Genet. Syst. 78: 427-432 Go to original source...
  47. VITTURI R., LANNINO A., MANSUETO C., MANSUETO V. & COLOMBA M. 2008: Silver-negative NORs in Pamphagus ortolaniae (Orthoptera: Pamphagidae). Eur. J. Entomol. 105: 35-39 Go to original source...
  48. WARCHALOWSKA-SLIWA E. 1998: Karyotype characteristics of katydid orthopterans (Ensifera, Tettigoniidae) and remarks on their evolution at different taxonomic levels. Folia Biol. (Krakow) 46: 143-176
  49. WARCHALOWSKA-SLIWA E. & MARYANSKA-NADACHOWSKA A. 1992: Karyotypes, C-bands, NORs location in spermatogenesis of Isophya brevipennis Brunner (Orthoptera: Phaneropteridae). Caryologia 45: 83-89 Go to original source...
  50. WARCHALOWSKA-SLIWA E., MARYANSKA-NADACHOWSKA A. & BUGROV A.G. 1992: Karyotypes, C-heterochromatin, and NOR in three species of the genus Gampsocleis Fieb. (Orthoptera: Tettigonioidea: Decticinae). Folia Biol. (Krakow) 40: 119-127
  51. WARCHALOWSKA-SLIWA E., BUGROV A.G. & MARYANSKANADACHOWSKA A. 1994: Karyotypes, C-banding pattern, and NORs of the genus Montana Zeuner 1941 (Orthoptera, Tettigonioidea, Decticinae). Folia Biol. (Krakow) 42: 89-94
  52. WARCHALOWSKA-SLIWA E., HELLER K.-G. & MARYANSKANADACHOWSKA A. 2005: Cytogenetic variability of European Tettigoniinae (Orthoptera, Tettigoniidae): Karyotypes, C-and Ag-NOR-banding. Folia Biol. (Krakow) 53: 161-171 Go to original source...
  53. WARCHALOWSKA-SLIWA E., MARYANSKA-NADACHOWSKA A. & HELLER K.-G. 2007: Cytogenetic variability of the genus Saga Charp. (Orthoptera, Tettigoniidae, Saginae): Heterochromatin distribution. Caryologia 60: 29-36
  54. WHITING M.F., CARPENTER J.C., WHEELER Q.D. & WHEELER W. C. 1997: The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. System. Biol. 46: 1-68
  55. ZACARO A.A., PROENCA S.J.R., LOPEZ-ANDRADE C. & SERRANO A.R.M. 2004: Cytogenetic analysis of Ctenostomini by C-banding and rDNA localization and its relevance to the knowledge of the evolution of tiger beetles (Coleoptera: Cicindelidae). Genetica 122: 261-268 Go to original source...