Eur. J. Entomol. 112 (3): 419-425, 2015 | DOI: 10.14411/eje.2015.063

First report on a multiple sex chromosome system (X1X2X30) and population variations in the frequency of ring bivalents in Pyrrhocoridae (Hemiptera: Heteroptera)

Harbhajan KAUR, Kalchana GABA
Department of Zoology and Environmental Sciences, Punjabi University, Patiala-147002, India; e-mail: harbhajankaur@hotmail.com

The family Pyrrhocoridae (Hemiptera: Heteroptera) is characterized by a modal diploid chromosome number of 16 (♂) ranging from 12 to 33 and simple (X0), multiple (X1X20) and neo-sex chromosome systems (neoX-neoY). Out of about 340 known species, only 22 species belonging to 7 genera have to date been cytogenetically analysed. In the present study, the chromosome complement and meiotic details of one species, Odontopus nigricornis Stål has been revised, whilst that of another species, Antilochus russus Stål has been cytogenetically analyzed for the first time. The diploid chromosome complement of O. nigricornis is 2n (♂) = 25 = 22A + X1X2X30; the first time this particular multiple sex chromosome system has been reported in the Pyrrhocoridae. Three sex chromosomes mostly remain intimately associated during male meiosis and their number was confirmed at diplotene and anaphase II, where they dissociate slightly to become distinct. Meiosis is post-reductional for sex chromosomes. However, unlike other pyrrhocorids with multiple X chromosomes, the X1, X2 and X3 lie outside the autosomal ring on the metaphase plate during both divisions. The male diploid chromosome complement of A. russus was found to be 2n = 27 = 26A + X0. Apart from the typical meiotic features of heteropterans, the latter species shows inter- and intra-population variations in frequency of ring bivalents.

Keywords: Heteroptera, Pyrrhocoridae, chromosomes, male meiosis, multiple Xs, ring bivalents, population variation

Received: December 23, 2014; Revised: April 15, 2015; Accepted: April 15, 2015; Prepublished online: May 15, 2015; Published: July 15, 2015  Show citation

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KAUR, H., & GABA, K. (2015). First report on a multiple sex chromosome system (X1X2X30) and population variations in the frequency of ring bivalents in Pyrrhocoridae (Hemiptera: Heteroptera). EJE, 112(3), 419-425. doi: 10.14411/eje.2015.063
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    References

    1. Banerjee M.K. 1958: A study of the chromosomes during meiosis in twenty eight species of Hemiptera (Heteroptera, Homoptera). - Proc. Zool. Soc. Calcutta 11: 9-37.
    2. Bansal N. 2012: Cytogenetic Investigations on Some Members of Family Coreidae (Insecta: Hemiptera: Heteroptera). Ph.D. Thesis, Punjabi University, Patiala, 328 pp.
    3. Bansal N. & Kaur H. 2013: Karyological and meiotic studies in seven species of Coreinae (Hemiptera: Heteroptera: Coreidae) from North India. - Zootaxa 3641: 577-586. Go to original source...
    4. Bardella V.B., Grazia J., Fernandes J.A.M. & Vanzela A.L.L. 2014: High diversity in CMA3/DAPI-banding patterns in heteropterans. - Cytogenet. Genome Res. 142: 46-53.  Go to original source...
    5. Battaglia E. 1956: A new type of segregation of the sex chromosomes in Dysdercus koenigii Fabr. (Hemiptera: Pyrrhocoridae). A critical note. - Caryologia 8: 205-213. Go to original source...
    6. Bressa M.J., Papeschi A.G., Mola L.M. & Larramendy M.L. 1998: Meiotic studies in Largus rufipennis (Castelnau) (Largidae, Heteroptera) II. Reciprocal translocations heterozygosity. - Heredity 51: 253-264. Go to original source...
    7. Bressa M.J., Papeschi A.G., Mola L.M. & Larramendy M.L. 1999: Meiotic studies in Dysdercus Guérin Méneville 1831 (Heteroptera: Pyrrhocoridae). I. Neo-XY in Dysdercus albofasciatus Berg 1878, a new sex chromosome determining system in Heteroptera. - Chromos. Res. 7: 503-508. Go to original source...
    8. 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...
    9. Bressa M.J., Fumagalli E., Ituarte S., Frassa M.V. & Larramendy M.L. 2002a: Meiotic studies in Dysdercus Guérin Méneville 1831 (Heteroptera: Pyrrhocoridae). II. Evidence on variations of the diffuse stage between wild and laboratory-inbred populations of Dysdercus chaquensis Freiberg, 1948. - Hereditas 137: 125- 131. Go to original source...
    10. Bressa M.J., Papeschi A.G. & Larramendy M.L. 2002b: Meiotic studies in Lygaeus alboornatus Blanchard (Heteroptera, Lygaeidae: Lygaeinae). - Caryologia 55: 15-19. Go to original source...
    11. Bressa M.J., Papeschi A.G., Fumagalli E., Van Doesburg P.H. & Larramendy M.L. 2003: Cytogenetic and nucleolar meiotic cycle analyses in Dysdercus imitator Blöte, 1931 (Pyrrhocoridae, Heteroptera) from Argentina. - Folia Biol. (Kraków) 51: 135-141.
    12. Bressa M.J., Papeschi A.G., Vítková M., Kubíčková S., Fuková I., Pigozzi M.I. & Marec F. 2009: Sex chromosome evolution in cotton stainers of the genus Dysdercus (Heteroptera: Pyrrhocoridae). - Cytogenet. Genome Res. 125: 292-305. Go to original source...
    13. Camacho J.P.M., Belda J. & Cabrero J. 1985: Meiotic behavior of the holocentric chromosomes of Nezara viridula (Insecta, Heteroptera) analyzed by C-banding and silver impregnation. - Can. J. Genet. 27: 490-497. Go to original source...
    14. Carr D.H. & Walker J.E. 1961: Carbol-fuchsin as a stain for human chromosomes. - Stain Technol. 30: 233-236. Go to original source...
    15. Cattani M.V. & Papeschi A.G. 2004: Nucleolus organizing regions and semi persistent nucleolus during meiosis in Spartocera fusca (Thunberg) (Coreidae, Heterotpera). - Hereditas 140: 105-111. Go to original source...
    16. 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...
    17. Fossey A. & Liebenberg H. 1995: Meiosis and nucleolar structures in the stink bug Carlisis wahlbergi Stål (Coreidae: Heteroptera). - Cytobios 81: 7-15.
    18. Franco M.J., Bressa M.J. & Papeschi A.G. 2006: Karyotype and male meiosis in Spartocera batalas and meiotic behavior ofmultiple sex chromosomes in Coreidae (Heteroptera). - Eur. J. Entomol. 103: 9-16. Go to original source...
    19. Grozeva S., Nokkala S. & Simov N. 2006: First evidence of sex chromosomes pre-reduction in male meiosis in the Miridae bugs (Heteroptera). - Folia Biol. (Krakow) 54: 9-12. Go to original source...
    20. Henderson S.A. 1962: Temperature and chiasma formation in Schistocerca gregaria II. Cytological effects of 40°C and the Mechanism for heat induced univalence. - Chromosoma 13: 437-463. Go to original source...
    21. Henry T.J. 2009: Biodiversity of Heteroptera. In Footit R.G.& Adler P.H. (eds): Insect Biodiversity: Science and Society. Wiley-Blackwell, Chichester, pp. 223-263. Go to original source...
    22. Jacobs D.H. & Liebenberg H. 2001: Cytogenetics of Adamanotus uncotibialis Jacobs (Heteroptera: Aradidae). - Caryologia 54: 83-96. Go to original source...
    23. Jones G.H. 1987: Chiasmata. In Moens P.B. (ed.): Meiosis. Academic Press, London, pp. 213-244. Go to original source...
    24. Kaur H. & Bansal N. 2012a: First cytogenetic report on seven species of Coreidae (Heteroptera) with a bibliographic review of chromosomal data. - J. Biol. Res. (Thessaloniki) 18: 235-248.
    25. Kaur H. & Bansal N. 2012b: Meiotic behavior of chromosomes in two species of Coreinae (Coreidae: Heteroptera). - Cytologia 77: 373-379. Go to original source...
    26. Kuznetsova V.G. 1988: The unusual mechanism of sex chromosome determination in the cotton bug Dysdercus superstitiosus F. (Pyrrhocoridae, Heteroptera). - Dokl. Akad. Nauk SSSR 301: 456-458.
    27. Lanzone C. & Souza M. 2006: Chromosome complement and meiosis in three species of the Neotropical bug genus Antiteuchus (Heteroptera: Pentatomidae: Discocephalinae). - Genet. Mol. Biol. 29: 49-55. Go to original source...
    28. 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.
    29. Manna G.K. 1957: Sex mechanism in Dysdercus. - Curr. Sci. 6: 187.
    30. Manna G.K. 1984: Chromosomes in evolution in Heteroptera. In Sharma A.K. & Sharma A. (eds): Chromosomes in Evolution of Eukaryotic Groups. CRC Press, Boca Raton, pp. 189-225.
    31. Manna G.K. & Deb Mallick S. 1981: Meiotic chromosome constitution in forty one species of Heteroptera. - Chromos. Inform. Serv. 31: 9-11.
    32. Mendes L.O.T. 1947: Sôbre a meiose de Dysdercus mendesi Blöete (1937), Hemiptera, Pyrrhocoridae. - Bragantia 7: 243-256. Go to original source...
    33. Mendes L.O.T. 1949: Observações citológicas em Dysdercus. Cadeias de cromossômios em tecido somático de Dysdercus mendesi Blöete (Hemiptera: Pyrrhocoridae). - Bragantia 9: 53-57. Go to original source...
    34. Mola L.M & Papeschi A.G. 1993: Meiotic studies in Largus rufipennis (Castelnau) (Largidae, Heteroptera). Frequency and behaviour of ring bivalents and B chromosomes. - Heredity 71: 33-40. Go to original source...
    35. Mola L.M. & Papeschi A.G. 1997: Citogenética de Dysdercus chaquensis (Heteroptera: Pyrrhocoridae). - Revta Soc. Entomol. Argent. 56: 20.
    36. Papeschi A.G. & Bressa M.J. 2006: Evolutionary cytogenetics in Heteroptera. - J. Biol. Res. 5: 3-21.
    37. Papeschi A.G., Mola L.M., Bressa M.J., Greizerstein E.J.V. & Poggio L. 2003: Behaviour of ring bivalents in holocentric systems: alternate sites of spindle attachment in Pachylis argentinus and Nezara virudula (Heteroptera). - Chromos. Res. 11: 725-733. Go to original source...
    38. Parshad R. 1957: Cytological studies in Heteroptera II. Chromosome complement and meiosis in the males of three pyrrhocorid bugs. - Cytologia 22: 127-135. Go to original source...
    39. Piza S.D.T. 1947a: Comportamento dos cromossômios sexuais de Dysdercus mendesi na segunda divisão dos espermatócitos. - Bragantia 7: 269-271. Go to original source...
    40. Piza S.D.T. 1947b: Cromossômios de Dysdercus (Hemiptera: Pyrrhocoridae). - Anais Esc. Super. Agric. "Luiz de Queiroz" 4: 209-216. Go to original source...
    41. Piza S.D.T. 1951: Interpretacão do typo sexual de "Dysdercus mendesi" Blöete (Hemiptera Pyrrhocoridae). - Genét. Ibér. 3: 107-112.
    42. Ray-Chaudhuri S.P. & Banerjee M.R. 1959: On the problem of sex-determination in the cotton stainer Dysdercus koenigii (Fabr.) (Pyrrhocoridae: Heteroptera). - Nucleus 2: 209-214.
    43. Ray-Chaudhuri S.P. & Manna G.K. 1952: A new type of segregation of the sex chromosomes in the meiotic divisions of the cotton stainer, Dysdercus koenigii (Fabr.). - J. Genet. 51: 191-197. Go to original source...
    44. Rebagliati P.J., Mola L.M. & Papeschi A.G. 2001: Karyotype and meiotic behaviour of the holokinetic chromosomes of six Argentine species of the Pentatomidae (Heteroptera). - Caryologia 54: 339-347. Go to original source...
    45. Rebagliati P.J., 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...
    46. Redei D., Tsai J.F. & Yang M.M. 2009: Heteropteran Fauna of Taiwan: Cotton Stainers and their Relatives (Hemiptera: Heteroptera: Pyrrhocoroidea). National Chung Hsing University, Taiwan, 53 pp.
    47. Ruthmann A. & Dahlberg R. 1976: Pairing and segregation of the sex chromosomes in X1X2-males of Dysdercus intermedius with a note on the kinetic organization of heteropteran chromosomes. - Chromosoma 54: 89-97. Go to original source...
    48. Sands V.E. 1982: Cytological studies of the Coreidae and Alydidae (Hemiptera: Heteroptera) I. Male meiosis in the Malaysian species. - Caryologia 35: 291-305. Go to original source...
    49. Schuh R.T. & Slater J.A. 1995: True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. Cornell University Press, Ithaca, 349 pp.
    50. Sharma G.P. 1956: Sex mechanism in Dysdercus. - Curr. Sci. 25: 360.
    51. Sharma G.P., Sud G.C. & Parshad R. 1957: Chromosome complement and the sex mechanism in Dysdercus cingulatus (Pyrrhocoridae, Heteroptera). - Caryologia 9: 278-285. Go to original source...
    52. Souza H.V., Souza F.B., Maruyama S.R.C., Castonhole M.M.U. & Itoyama M.M. 2009: Meiosis, spermatogenesis and nucleolar behavior in the seminiferous tubules of Alydidae, Coreidae and Rhopalidae (Heteroptera) species. - Genet. Mol. Res. 8: 1383-1396. Go to original source...
    53. Suja J.A., Dalcerro A.J., Page J., Rufas J. & 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...
    54. Suman V. 2010: Cytological Studies on the Superfamily Lygaeoidea (Insecta: Hemiptera: Heteroptera). Ph.D. Thesis, Punjabi University, Patiala, 226 pp.
    55. Ueshima N. 1979: Hemiptera II: Heteroptera. In John B. (ed.): Animal Cytogenetics. Vol. 3. Insecta 6. Borntraeger, Berlin, v + 117 pp.
    56. Verma S. & Kurl S.P. 2009: Cytogenetical studies of a bug, Odontopus nigricornis Stål (Heteroptera: Pyrrhocoridae). - J. Exp. Zool. India 12: 443-446.

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