Eur. J. Entomol. 111 (2): 165-174, 2014 | DOI: 10.14411/eje.2014.027

Karyotype evolution in progress: A new diploid number in Belostoma candidulum (Heteroptera: Belostomatidae) from Argentina leading to new insights into its ecology and evolution

Mónica G. CHIRINO1,2, María J. BRESSA1
1 Instituto de Ecología, Genética y Evolución de Buenos Aires, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, C1428EHA, Ciudad Autónoma de Buenos Aires, Argentina; e-mails: mchirino@ege.fcen.uba.ar; mjbressa@ege.fcen.uba.ar
2 Laboratorio de Entomología Aplicada y Forense, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Roque Sáenz Peña 352, B1876BXD, Bernal, Buenos Aires, Argentina

A novel chromosome complement (2n = 14 = 12 + XY/XX; male/female sex chromosomes), male meiosis behaviour, heterochromatin characterization, and frequency and distribution of chiasmata are described for the first time in specimens from a natural population of the giant water bug, Belostoma candidulum Montandon, 1903 (Heteroptera: Belostomatidae) from Argentina. To date, specimens of B. candidulum have been reported by other authors in a sample from a natural population from Brazil. Our results demonstrate that Argentinean and Brazilian populations have different diploid numbers and chromosomal features. During male meiosis, autosomal bivalents generally show a single chiasma, behave as telokinetic chromosomes (i.e. kinetic activity is restricted to terminal regions), and divide reductionally at anaphase I; in contrast, the sex chromosomes are achiasmatic, behave as univalents and segregate equationally at anaphase I. Among autosomal bivalents of B. candidulum, one is remarkably larger and may present one or two terminal chiasmata, showing rod, V-shaped and ring configurations. Here we propose a new mode of segregation for ring bivalents, since it is not essential that one of the chiasmata is released during anaphase I because alternative sites for microtubule attachment become functional for the normal chromosome segregation to the poles. Heterochromatin content is very scarce in specimens from Argentinean B. candidulum populations, revealing C-positive interstitial and terminal dots in three pairs of autosomes and C-blocks at both ends of X chromosome, whereas the Y chromosome is mainly C-positive. One of the C-positive bands from X and Y chromosomes is DAPI-dull/CMA-bright, which could represent the nucleolus organizing region (NOR) detected by fluorescent in situ hybridization (FISH). The location of the NORs in both sex chromosomes allowed us to use them as a cytological marker to describe their behaviour during meiosis. Despite the fact that specimens from the Argentinean and Brazilian populations have been classified as a single species due to their morphological similarity, our results suggest that both populations are chromosomal races or even morphologically-identical cryptic species. The results obtained support the hypothesis that karyotype of B. candidulum originated through autosomal fusions and the fusion of the X and Y chromosomes with the ancestral NOR-autosomal pair. Lastly, the genus Belostoma represents an excellent model for assessing the main mechanisms involved in the karyotype evolution in organisms with holokinetic chromosomes, from which inferences may be made concerning its broader ecology and evolution.

Keywords: Heteroptera, Belostomatidae, Belostoma candidulum, holokinetic chromosomes, ring bivalents, chromosomal races, cryptic species, karyotype evolution, rDNA-FISH

Received: November 18, 2013; Revised: December 31, 2013; Accepted: December 31, 2013; Prepublished online: March 14, 2014; Published: May 5, 2014  Show citation

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CHIRINO, M.G., & BRESSA, M.J. (2014). Karyotype evolution in progress: A new diploid number in Belostoma candidulum (Heteroptera: Belostomatidae) from Argentina leading to new insights into its ecology and evolution. EJE, 111(2), 165-174. doi: 10.14411/eje.2014.027
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    References

    1. Analytycal Software 1998: Statistix for Windows. Version 2.0. Tallahassee, FL, USA
    2. Bardella V.B., Dias A.L., Giuliano-Caetano L., Ribeiro J.R.I. & Da Rosa R. 2012: Sex chromosome differentiation in Belostoma (Insecta: Heteroptera: Belostomatidae). - Genet. Mol. Res. 11: 2476-2486 Go to original source...
    3. Bressa M.J., Papeschi A.G., Mola L.M. & Larramendy M.L. 1998: Meiotic studies in Largus rufipennis (Castelnau) (Largidae, Heteroptera). II. Reciprocal translocation heterozygosity. - Caryologia 51: 253-264 Go to original source...
    4. 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...
    5. Bressa M.J., Papeschi A.G., Mola L.M. & Larramendy M.L. 2001: Autosomal univalents as a common meiotic feature in Jadera haematoloma (Herrich-Schaeffer, 1847) and Jadera sanguinolenta (Fabricius, 1775) (Heteroptera, Rhopalidae: Rhopalinae). - Eur. J. Entomol. 98: 151-157 Go to original source...
    6. Bressa M.J., Papeschi A.G., Mola L.M. & Larramendy M.L. 2002a: Meiotic studies in Lygaeus alboornatus Blanchard 1852 (Heteroptera: Lygaeidae: Lygaeinae). - Caryologia 55: 15-19 Go to original source...
    7. Bressa M.J., Fumagalli E., Ituarte S., Frassa M.V. & Larramendy M.L. 2002b: Meiotic studies in Dysdercus Guerin Meneville, 1831 (Heteroptera: Pyrrhocoridae). II. Evidence of variations in the diffuse stage between wild and laboratory inbred populations of Dysdercus chaquensis Freiberg, 1948. - Hereditas 137: 125-131 Go to original source...
    8. Bressa M.J., Larramendy M.L. & Papeschi A.G. 2005: Heterochromatin characterization in five species of Heteroptera. - Genetica 124: 307-317 Go to original source...
    9. Bressa M.J., Papeschi A.G., Vitkova M., Kubickova S., Fukova 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...
    10. 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...
    11. Cattani M.V. & Papeschi A.G. 2004: Nucleolus organizing regions and semi-persistent nucleolus during meiosis in Spartocera fusca (Thunberg) (Coreidae, Heteroptera). - Hereditas 140: 105-111 Go to original source...
    12. Cattani M.V., Greizerstein E.J. & Papeschi A.G. 2004: Male meiotic behaviour and nucleolus organizer regions in Camptischium clavipes (Fabr.) (Coreidae, Heteroptera) analyzed by fluorescent banding and in situ hybridization. - Caryologia 57: 267-273 Go to original source...
    13. Chirino M.G., Papeschi A.G. & Bressa M.J. 2013: The significance of cytogenetics for the study of karyotype evolution and taxonomy of water bugs (Heteroptera, Belostomatidae) native to Argentina. - Comp. Cytogenet. 7: 9-27 Go to original source...
    14. Criniti A., Simonazzi G., Cassanelli S., Ferrari M., Bizzaro D. & Manicardi G.C. 2009: Distribution of heterochromatin and rDNA on the holocentric chromosomes of the aphids Dysaphis plantaginea and Melanaphis pyraria (Hemiptera: Aphididae). - Eur. J. Entomol. 106: 153-157 Go to original source...
    15. Daniel W.W. 1990: Applied Nonparametric Statistics. PWS-Kent, Devon, UK, 635 pp
    16. Franco M., Bressa M.J. & Papeschi A.G. 2006: Karyotype and male meiosis in Spartocera batatas (Fabricius) and meiotic behaviour of multiple sex chromosomes in Coreidae, Heteroptera. - Eur. J. Entomol. 103: 9-16 Go to original source...
    17. Fukova I., Nguyen P. & Marec F. 2005: Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. - Genome 48: 1083-1092 Go to original source...
    18. Glaser R.W. 1917: Ringer solutions and some notes on the physiological basis of their ionic composition. - Comp. Biochem. Physiol. 2: 241-289 Go to original source...
    19. Heckman C.W. 2011: Belostomatidae. In: Encyclopedia of South American Aquatic Insects: Hemiptera - Heteroptera. Illustrated Keys to Known Families, Genera, and Species in South America. Springer, Dordrecht, Heidelberg, London, New York, pp. 393-434 Go to original source...
    20. Jacobs D.H. & Groenveld H.T. 2002: Cytogenetics and karyotype evolution of the genus Silvacoris Jacobs (Heteroptera: Aradidae: Carventinae) with a description of a statistical method to compare karyotypes. - Cytologia 67: 159-168 Go to original source...
    21. Jacobs D.H. & Liebenberg H. 2001: Cytogenetics of Adamanotus uncotibialis Jacobs (Heteroptera: Aradidae). - Caryologia 54: 83-86 Go to original source...
    22. Lockwood A.P.M. 1961: 'Ringer' solutions and some notes on the physiological basis of their ionic composition. - Comp. Biochem. Physiol. 2: 241-289 Go to original source...
    23. 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, FL, pp. 189-225
    24. McClung C.E. 1905: The chromosome complex of orthopteran spermatocytes. - Biol. Bull. 9: 304-340 Go to original source...
    25. Mola L.M. & Papeschi A.G. 1993: Meiotic studies in Largus rufipennis (Castelnau) (Largidae, Heteroptera): frequency and behaviour of ring bivalents, univalents and B chromosomes. - Heredity 71: 33-40 Go to original source...
    26. Motzko D. & Ruthmann A. 1984: Spindle membranes in mitosis and meiosis of the heteropteran insect Dysdercus intermedius. A study of the interrelationship of spindle architecture and the kinetic organization of chromosomes. - Eur. J. Cell Biol. 33: 205-216
    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. 1992: Estudios Citogeneticos y Evolutivos en Heteroptera. Doctoral Thesis, Universidad de Buenos Aires, 259 pp. [in Spanish]
    30. Papeschi A.G. 1994: Chromosome rearrangements in Belostoma plebejum (Stal) (Belostomatidae, Heteroptera). - Caryologia 47: 223-230 Go to original source...
    31. Papeschi A.G. 1995: Correspondence between C-banding and Ag-NOR in the sex chromosomes of Belostoma oxyurum (Belostomatidae, Heteroptera). - Cytologia 60: 291-295 Go to original source...
    32. Papeschi A.G. 1996: Sex chromosome polymorphism in species of Belostoma (Belostomatidae, Heteroptera). - Hereditas 124: 269-274 Go to original source...
    33. Papeschi A.G. & Bidau C.J. 1985: Chromosome complement and male meiosis in four species of Belostoma Latreille (Heteroptera: Belostomatidae). - Braz. J. Genet. 8: 249-261
    34. Papeschi A.G. & Bressa M.J. 2006: Evolutionary cytogenetics in Heteroptera. - J. Biol. Res. 5: 3-21
    35. Papeschi A.G., Mola L.M., Bressa M.J., Greizerstein E.J., Lia V. & Polhemus 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...
    36. Perez R., Calleros L., Rose V., Lorca M. & Panzera F. 2004: Cytogenetic studies on Mepraia gajardoi (Heteroptera: Reduviidae). Chromosome behaviour in a spontaneous translocation mutant. - Eur. J. Entomol. 101: 211-218 Go to original source...
    37. Poggio M.G., Bressa M.J. & Papeschi A.G. 2011: Male meiosis, heterochromatin characterization and chromosomal location of rDNA in Microtomus lunifer (Berg, 1900) (Hemiptera: Reduviidae: Hammacerinae). - Comp. Cytogenet. 5: 1-22 Go to original source...
    38. Polhemus J.T. & Polhemus D.A. 2008: Global diversity of true bugs (Heteroptera: Insecta) in freshwater. - Hydrobiologia 595: 379-391 Go to original source...
    39. Rebagliati P.J. & Mola L.M. 2010: Meiotic behavior and karyotypic variation in Acledra (Pentatomidae, Heteroptera). - Genet. Mol. Res. 9: 739-749 Go to original source...
    40. Rebagliati P.J., Mola L.M. & Papeschi A.G. 2001: Karyotype and meiotic behaviour of the holokinetic chromosomes of six Argentine species of Pentatomidae (Heteroptera). - Caryologia 54: 339-347 Go to original source...
    41. Rebagliati P.J., Papeschi A.G. & Mola L.M. 2003: Meiosis and fluorescent bandings in Edessa meditabunda and Edessa rufomarginata (Heteroptera: Pentatomidae: Edessinae). - Eur. J. Entomol. 100: 11-18 Go to original source...
    42. Reeves A. & Tear J. 2000: MicroMeasure for Windows, version 3.3. (Free program, distributed by the authors via http://www.colostate.edu/Depts/Biology/Micro-Measure)
    43. Ribeiro J.R. 2007: A review of the species of Belostoma Latreille, 1807 (Hemiptera: Heteroptera: Belostomatidae) from the four southeastern Brazilian states. - Zootaxa 1477: 1-70 Go to original source...
    44. Ribeiro J.R. & Estevez A.K. 2009: The small species of Belostoma Latreille (Heteroptera, Belostomatidae). III. A revision of oxyurum group, with a new species from Brazil and description of the male of B. noualhieri Montandon. - Rev. Bras. Entomol. 53: 207-215 Go to original source...
    45. Saez F.A. 1960: El empleo de la hematoxilina acetica o propionica para el estudio de los cromosomas con la tecnica de aplastamiento. - Com. Soc. Biol. Montevideo (Mimeographed): 1
    46. 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...
    47. Schnack J.A. 1976: Los Belostomatidae de la Republica Argentina (Hemiptera). In Ringuelet R.A. (ed.): Fauna de Agua Dulce de la Republica Argentina. Fundacion para la Educacion la Ciencia y la Cultura, Buenos Aires, pp. 1-66
    48. 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...
    49. Thomas D.B.J. 1987: Chromosome evolution in the Heteroptera (Hemiptera): agmatoploidy versus aneuploidy. - Ann. Entomol. Soc. Am. 80: 720-730 Go to original source...
    50. Traut W. 1976: Pachytene mapping in the female silkworm Bombyx mori L. (Lepidoptera). - Chromosoma 58: 275-284 Go to original source...
    51. Ueshima N. 1979: Hemiptera II: Heteroptera. In John B. (ed.): Animal Cytogenetics. Vol. 3. Insecta 6. Borntraeger, Berlin, v + 117 pp

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