Eur. J. Entomol. 103 (1): 9-16, 2006 | DOI: 10.14411/eje.2006.002

Karyotype and male meiosis in Spartocera batatas and meiotic behaviour of multiple sex chromosomes in Coreidae (Heteroptera)

María José FRANCO1, María José BRESSA1,2, Alba GRACIELA PAPESCHI*,1,2
1 Laboratorio de Citogenética y Evolución, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina; e-mail: alpape@ege.fcen.uba.ar
2 Members of the Carrera del Investigador Científico (CONICET)

The Coreidae (Heteroptera) have holokinetic chromosomes and during male meiosis the autosomal bivalents segregate reductionally at anaphase I while the sex chromosomes do so equationally. The modal diploid chromosome number of the family is 2n = 21, with a pair of m-chromosomes and an X0/XX sex chromosome system. A 2n = 24/26 (male/female) and an X1X20/X1X1X2X2 sex chromosome system were found in Spartocera batatas (Fabricius). C-banding and fluorescent-banding revealed the presence of AT-rich heterochromatic bands medially located on all the autosomes, and one telomeric band on both the X1 and X2 chromosomes. This banding pattern differed from the telomeric heterochromatin distribution found in most other heteropteran species. The X1 and X2 chromosomes were intimately associated during male meiosis and difficult to recognize as two separate entities. Based on a comparison with the behaviour of sex chromosomes in other coreids and other heteopterans with multiple sex chromosomes it is suggested that the particular behaviour of X1 and X2 chromosomes in coreid species with multiple sex chromosome systems evolved as an alternative mechanism for ensuring the proper segregation of the sex chromosomes during meiosis.

Keywords: Holokinetic chromosomes, multiple sex chromosomes, C-banding, fluorescent-banding, karyotype evolution, Heteroptera

Received: August 22, 2005; Revised: October 16, 2005; Accepted: October 16, 2005; Published: January 30, 2006  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
FRANCO, M.J., BRESSA, M.J., & GRACIELA PAPESCHI, A. (2006). Karyotype and male meiosis in Spartocera batatas and meiotic behaviour of multiple sex chromosomes in Coreidae (Heteroptera). EJE103(1), 9-16. doi: 10.14411/eje.2006.002
Download citation

References

  1. ANGUS R.B., KEMENY C.K. & WOOD E.L. 2004: The C-banded karyotypes of the four British species of Notonecta L. (Heteroptera: Notonectidae). Hereditas 140: 134-138 Go to original source...
  2. BRESSA M.J., PAPESCHI A.G., MOLA L.M. & LARRAMENDY M.L. 1999: Meiotic studies in Dysdercus Guerin Meneville 1831 (Heteroptera: Pyrrhocoridae). I. Neo-XY in Dysdercus albofasciatus Berg 1878, a new sex chromosome determining system in Heteroptera. Chromosome Res. 7: 503-508 Go to original source...
  3. BRESSA M.J., PAPESCHI A.G., MOLA L.M. & LARRAMENDY M.L. 2001: Autosomal univalents as a common meiotic feature in Jadera haematoloma and Jadera sanguinolenta (Heteroptera: Rhopalidae: Serinethinae). Eur. J. Entomol. 98: 151-157 Go to original source...
  4. BRESSA M.J., PAPESCHI A.G., FUMAGALLI E., VAN DOESBURG P.H. & LARRAMENDY M. 2003: Cytogenetic and nucleolar meiotic cycle analyses in Dysdercus imitator BlGte, 1931 (Heteroptera, Pyrrhocoridae) from Argentina. Folia Biol. 51: 135-141
  5. BRESSA M.J., LARRAMENDY M. & PAPESCHI A.G. 2005: Heterochromatin characterization in five species of Heteroptera. Genetica 124: 307-317 Go to original source...
  6. CAMACHO J.P.M., BELDA J. & CABRERO J. 1985: Meiotic behaviour of the holocentric chromosomes of Nezara viridula (Insecta, Heteroptera) analysed by C-banding and silver impregnation. Can. J. Genet. Cytol. 27: 490-497 Go to original source...
  7. CATTANI M.V. & PAPESCHI A.G. 2004: Nucleolus organizing regions and semipersistent nucleolus during meiosis in Spartocera fusca (Thurnberg) (Coreidae, Heteroptera). Hereditas 140: 105-111 Go to original source...
  8. CATTANI M.V., GREIZERSTEIN E.J. & PAPESCHI A.G. 2004: Male meiotic behaviour and nucleolus organizing regions in Camptischium clavipes (Fabr.) (Coreidae, Heteroptera) analyzed by fluorescent banding and in situ hybridization. Caryologia 57: 267-273 Go to original source...
  9. DEY S.K. & WANGDI T. 1990: Banding patterns of the holocentric chromosomes in some species of Heteroptera. Cytologia 55: 181-186 Go to original source...
  10. DUTT M.K. 1957: Cytology of three species of coreid bugs with special reference to multiple sex chromosome mechanism. Genetica 29: 110-119 Go to original source...
  11. FOSSEY A. & LIEBENBERG H. 1995: Meiosis and nucleolar structures in the stink bug Carlisis wahlbergi Stal (Coreidae: Heteroptera). Cytobios 81: 7-15
  12. GARCIA TAVARES M. & VILELA DE AZEREDO-OLIVEIRA M.T. 1997: Pattern of nucleolar activity during spermiogenesis in triatomines (Heteroptera, Reduviidae) as analysed by silver staining. Cytobios 89: 93-103
  13. GONZALEZ-GARCIA J.M., ANTONIO C., SUJA J.A. & RUFAS J.S. 1996: Meiosis in holocentric chromosomes: kinetic activity is randomly restricted to the chromatid ends of sex univalents in Graphosoma italicum (Heteroptera). Chromosome Res. 4: 124-132 Go to original source...
  14. GROZEVA S. & NOKKALA S. 2001: Chromosome numbers, sex determining systems, and patterns of the C-heterochromatin distribution in 13 species of lace bugs (Heteroptera, Tingidae). Folia Biol. 49: 29-41
  15. GROZEVA S. & NOKKALA S. 2003: C-heterochromatin and extra (B) chromosome distribution in six species of the Nabis (Heteroptera, Nabidae) with the modal male karyotype 2n = 16 + XY. Folia Biol. 51: 13-21
  16. GROZEVA S., KUZNETSOVA V.G. & NOKKALA S. 2004: Patterns of chromosome banding in four nabid species (Heteroptera, Cimicomorpha, Nabidae) with high chromosome number karyotypes. Hereditas 140: 99-104 Go to original source...
  17. HEITZ E. 1933: Die somatischen Heteropyknose bei Drosophila melanogaster und ihre genetische Bedeutung. Z. Zellforsch. 20: 237-287 Go to original source...
  18. HEITZ E. 1935: Die Herkunft der Chromozentren. Planta 18: 571-635 Go to original source...
  19. ITUARTE S. & PAPESCHI A.G. 2004: Achiasmatic male meiosis in Tenagobia (Fuscagobia) fuscata (Heteroptera, Corixoidea, Micronectidae). Genetica 122: 199-206 Go to original source...
  20. JACOBS D.H. 2004: The evolution of a neo-XY1Y2 sex chromosome system by autosome-sex chromosome fusion in Dundocoris nodulicarinus Jacobs (Heteroptera: Aradidae: Carventinae). Chromosome Res. 12: 175-191 Go to original source...
  21. MANNA G.K. 1951: A study of the chromosomes during meiosis in forty-three species of Indian Heteroptera. Proc. Zool. Soc. Bengal 4: 1-116
  22. MANNA G.K. 1984: Chromosomes in evolution in Heteroptera. In Sharma A.K. & Sharma A. (ed.): Chromosomes in Evolution of Eukaryotic Groups. CRC Press, Boca Raton, FL, pp 189-225
  23. MANNA G.K., UESHIMA N., DEY S.K. & DEB-MALLIK S. 1985: Marked sex chromosomal variations between Indian and Japanese species of Physopelta (Largidae, Heteroptera). Cytologia 50: 621-630 Go to original source...
  24. NOKKALA S. 1986: The mechanisms behind the regular segregation of the m chromosomes in Coreus marginatus L. (Coreidae, Hemiptera). Hereditas 105: 73-85 Go to original source...
  25. PANZERA F., PEREZ R., PANZERA Y., ALVAREZ F., SCVORTZOFF E. & SALVATELLA R. 1995: Karyotype evolution in holocentric chromosomes of three related species of triatomines (Hemiptera: Reduviidae). Chromosome Res. 3: 143-150 Go to original source...
  26. PANZERA F., HORNOS S., PEREIRA J., CESTAU R., CANALE D., DIOTAIUTI L., DUJARDIN J.P. & PEREZ R. 1997: Genetic variability and geographic differentiation among three species of triatominae bugs (Hemiptera: Reduviidae). Am. J. Trop. Med. Hyg. 57: 732-739 Go to original source...
  27. PAPESCHI A.G. 1988: C-banding and DNA content in three species of Belostoma (Heteroptera) with large differences in chromosome size and number. Genetica 76: 43-51 Go to original source...
  28. PAPESCHI A.G. 1991: DNA content and heterochromatin variation in species of Belostoma (Heteroptera, Belostomatidae). Hereditas 115: 109-114 Go to original source...
  29. PAPESCHI A.G. 1994: Chromosome rearrangements in Belostoma plebejum (Belostomatidae, Heteroptera). Caryologia 47: 223-230 Go to original source...
  30. PAPESCHI A.G. 1996: Sex chromosome polymorphism in species of Belostoma (Belostomatidae, Heteroptera). Hereditas 124: 269-274 Go to original source...
  31. PAPESCHI A.G. & BRESSA M.J. (in press): Evolutionary cytogenetics in Heteroptera. J. Biol. Res
  32. PAPESCHI A.G., MOLA L.M., BRESSA M.J., GREIZERSTEIN E.J., LIA V. & POGGIO L. 2003: Behaviour of ring bivalents in holokinetic systems: alternative sites of spindle attachment in Pachylis argentinus and Nezara viridula (Heteroptera). Chromosome Res. 11: 725-733 Go to original source...
  33. PARSHAD R. 1957: Chromosome number and sex mechanism in twenty species of the indian Heteroptera. Curr. Sci. 16: 125.
  34. PIGOZZI M.I. & SOLARI A.J. 2003: Differential immunolocalization of a putative Rec8p in meiotic autosomes and sex chromosomes of triatomine bugs. Chromosoma 112: 38-47 Go to original source...
  35. REBAGLIATI P., PAPESCHI A.G. & MOLA L.M. 2003: Meiosis and fluorescent banding in Edessa meditabunda and E. rufomarginata (Heteroptera: Pentatomidae: Edessinae). Eur. J. Entomol. 100: 11-18 Go to original source...
  36. REBAGLIATI P., MOLA L.M., PAPESCHI A.G. & GRAZIA J. 2005: Cytogenetic studies in Pentatomidae (Heteroptera): A review. J. Zool. Syst. Evol. Res. 43: 199-213 Go to original source...
  37. SCHAEFER C.W. & PANIZZI A.R. 2000: Heteroptera of Economic Importance. CRC Press, Boca Raton, FL, 828 pp Go to original source...
  38. SCHUH R.T. & SLATER J. 1995: True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. Cornell University Press, New York, 349 pp
  39. SOLARI A.J. 1979: Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae; Hemiptera). Chromosoma 72: 225-240 Go to original source...
  40. SUJA J.A., DEL CERRO A.L., PAGE J., RUFAS J.S. & SANTOS J.L. 2000: Meiotic sister chromatid cohesion in holocentric sex chromosomes of three heteropteran species is maintained in absence of axial elements. Chromosoma 109: 35-43 Go to original source...
  41. UESHIMA N. 1979: Hemiptera II: Heteroptera. In John B. (ed.): Animal Cytogenetics. Gebrueder Borntraeger, Berlin, Stuttgart, v + 117 pp
  42. WILSON E.B. 1907: The supernumerary chromosomes of Hemiptera. Science 26: 870-871 Go to original source...
  43. WILSON E.B. 1909: Studies on chromosomes. V. The chromosomes of Metapodius. A contribution to the hypothesis of the genetic continuity of chromosomes. J. Exp. Zool. 6: 147-205 Go to original source...
  44. XAVIER A. 1945: Cariologia comparada de alguns Hemipteros Heteropteros (Pentatomoideos e Coreideos). Mem. Estud. Mus. Zool. Univ. Coimbra 163: 1-105

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.