Eur. J. Entomol. 112 (1): 1-10, 2015 | 10.14411/eje.2015.024

Different steps in the evolution of neo-sex chromosomes in two East African Spalacomimus species (Orthoptera: Tettigoniidae: Hetrodinae)

Elżbieta WARCHAŁOWSKA-ŚLIWA1, Beata GRZYWACZ1, Anna MARYAŃSKA-NADACHOWSKA1, Andreas HEMP2, Claudia HEMP3
1 Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland; e-mails: warchalowska@isez.pan.krakow.pl; grzywacz@isez.pan.krakow.pl; maryanska@isez.pan.krakow.pl
2 Department of Plant Systematics, University of Bayreuth, Germany; e-mail: andreas.hemp@uni-bayreuth.de
3 Department of Animal Ecology and Tropical Biology (Zoology III), University of Würzburg, Germany; e-mail: claudia.hemp@uni-wuerzburg.de

Two orthopteran species belonging to the East African genus Spalacomimus, S. verruciferus and S. talpa (Tettigoniidae: Hetrodinae), were investigated using both molecular cytogenetic techniques, including fluorescence in situ hybridization with 18S rDNA and (TTAGG)n telomeric probes, and classical techniques, such as C-banding, fluorochrome CMA3/DAPI staining, and silver impregnation. These techniques allowed us to identify cytogenetic markers that were then used to elucidate chromosome organization and differences between species. Chromosomal complements are reported for the first time for both analyzed species, which showed the same chromosomal number of 2n = 24 and the neo-XY sex chromosome system; however, the morphology of neo-sex chromosomes differs between these species. A cluster of the major rDNA (i.e., the nucleolar organizer region, NOR) was found to be located in the interstitial region of the sex chromosomes of S. verruciferus, whereas it was on the long pair of autosomes in S. talpa. The difference between the karyotypes of the studied species indicate divergent origins of their neo-XY systems. A detailed description of the structure and behaviour of the sex chromosome configuration in male meiosis is provided. In S. verruciferus, the neo-XY system is derived from a Robertsonian fusion between the original acrocentric X and an acrocentric long pair of autosomes bearing an rDNA/NOR locus, leading to a bi-armed X and an acrocentric neo-Y chromosome. The neo-XY in S. talpa arose due to complicated rearrangements, attributable to a tandem fusion between the original acrocentric X and part of a medium-sized autosome, and resulting in supernumerary chromosomes. In the latter case, behaviour of the neo-X and neo-Y demonstrates a post-reductional division of these chromosomes. Variation in the evolution of two neo-XY sex chromosome systems are novel phylogenetic markers for the Hetrodinae and seem to promote speciation as important aspect for taxonomy.

Keywords: Orthoptera, Tettigoniidae, Spalacomimus, karyotype evolution, neo-XY

Received: July 2, 2014; Accepted: October 23, 2014; Prepublished online: December 5, 2014; Published: January 25, 2015

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References

  1. Alicata P., Messina A. & Oliveri S. 1974: Determinismo cromosomico del sesso in Odontura stenoxipha (Orth., Phaneropteridae): un nuovo casa di neo-XY. - Animalia 1: 109-122
  2. Ashley T., Jaarola M. & Fredga K. 1989: Absence of synapsis during pachynema of the normal sized sex chromosomes of Microtus arvalis. - Hereditas 111: 295-304 Go to original source...
  3. Brown J.D. & O Neill R.J. 2010: Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. - Annu. Rev. Genomics Hum. Genet. 11: 291-316 Go to original source...
  4. 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...
  5. Bugrov A.G. & Warchalowska-Sliwa E. 1997: Chromosome numbers and C-banding patterns in some Pamphagidae grasshoppers (Orthoptera, Acrididae) from the Caucasus, Central Asia, and Transbaikalia. - Folia Biol. (Krakow) 45: 133-138
  6. Cabrero J. & Camacho J.P.M. 2008: Location and expression of ribosomal RNA genes in grasshoppers: Abundance of silent and cryptic loci. - Chromosome Res. 16: 595-607 Go to original source...
  7. Cabrero J., Bakkali M., Bugrov A.G., Warchalowska-Sliwa E., Lopez-Leon M.D., Perfectti F. & Camacho J.P.M. 2003: Multiregional origin of B chromosomes in the grasshopper Eyprepocnemis plorans. - Chromosoma 112: 207-211 Go to original source...
  8. Camacho J.P.M., Orozco J.C. & Pascual F. 1981: Chromosomal rearrangements and karyotype evolution in Decticinae (Orthoptera: Tettigonioidea). - Cytologia 46: 209-215 Go to original source...
  9. Camacho J.P.M., Sharbel T.F. & Beukeboom L.W. 2000: B-chromosome evolution. - Phil. Trans. R. Soc. Lond. (B) 355: 163-178 Go to original source...
  10. Castillo E.R.D., Marti D.A. & Bidau C.J. 2010: Sex and neo-sex chromosomes in Orthoptera: a review. - J. Orthopt. Res. 19: 213-231 Go to original source...
  11. Chopard L. & Kevan D.K. McE. 1954: Orthoptera - Ensifera from northern Kenya and Jubaland. - Tran. R. Entomol. Soc. Lond. 105: 315-353 Go to original source...
  12. Dave M.J. 1965: On unusual sex chromosomes found in two species of the Locustidae. - Cytologia 30: 194-200 Go to original source...
  13. Faria R. & Navarro A. 2010: Chromosomal speciation revisited: rearranging theory with pieces of evidence. - Trends Ecol. Evol. 25: 660-669 Go to original source...
  14. Favrelle M. 1936: Contribution a l etude de la garniture chromosomique des Orthopteres (Gryllidae et Tettigoniidae). - Mem. Mus. R. Hist. Nat. Belg. (Ser. 2) 3: 53-60
  15. Ferreira A. 1969: Chromosome survey of some Australian tettigoniids (Orthoptera, Tettigonioidea): Two species with neo-XY sex determining mechanism. - Cytologia 34: 511-522 Go to original source...
  16. Ferreira A. 1976: Cytology of Brazilian Phaneropteridae (Orthoptera, Tettigonnioidea): a species with neo XY sex determining mechanism. - Can. J. Genet. Cytol. 18: 79-84 Go to original source...
  17. Fernandez-Piqueras J., Rojo Garcia E. & Sentis Castano C. 1981: A tandem fusion origin of a neo XY sex determining mechanism in the long-horned Callicrania seoanei (Bol.). - Heredity 48: 147-150 Go to original source...
  18. Fernandez-Piqueras J., Rodriguez Camos A., Sentis Castano C. & Wandosell Jurado F. 1982: Pycnogaster cucullata (Charp.): a polytypic species of Tettigonioidea with X0 and neo XY sex determination. - Heredity 48: 147-150 Go to original source...
  19. Grzywacz B., Chobanov D.P., Maryanska-Nadachowska A., Karamysheva T.V., Heller K.-G. & Warchalowska-Sliwa E. 2014: A comparative study of genome organization and inferences for the systematics of two large bushcricket genera of the tribe Barbitistini (Orthoptera: Tettigoniidae: Phaneropterinae). - BMC Evol. Biol. 14: 48 Go to original source...
  20. Hemp C. 2013: Annotated list of Ensifera (Orthoptera) and further records on Caelifera (Orthoptera) of Mt Kilimanjaro, Tanzania. - Zootaxa 3613: 301-342 Go to original source...
  21. Kitano J. & Peichel C.L. 2012: Turnover of sex chromosome and speciation in fishes. - Environ. Biol. Fishes 94: 549-558 Go to original source...
  22. Kral J., Musilova J., Stahlavsky F., Rezac M., Akan Z., Edwards R.L., Coyle F.A. & Almerje C.B. 2006: Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spider (Aranea: Araneomorphae). - Chromosome Res. 14: 859-880 Go to original source...
  23. Kuznetsova V.G., Grozeva S.M., Nokkala S. & Nokkala C. 2011: Cytogenetics of the true bug infraorder Cimicomorpha (Hemiptera, Heteroptera): a review. - ZooKeys 154: 31-70 Go to original source...
  24. Matthey R. 1948: Donnees nouvelles sur les chromosomes des Tettigonides et la parthenogenese de Saga pedo Pallas. - Rev. Suisse Biol. 55: 45-56
  25. Mbata K.J. 2005: A contribution to the cytogenetics of the armoured ground cricket, Acanthoplus speiseri (Orthoptera: Tettigoniidae), a pest of grain crops in Zambia. - Int. J. Trop. Insect Sci. 25: 142-145 Go to original source...
  26. Messina A. 1981: Sulle specie di Odontura del gruppo Stenoxypha (Fieb.) (Orthoptera, Phaneropterinae). - Animalia 8: 15-23
  27. Megias-Nogales B., Marchal J.A., Acosta M.J., Bullejos M., Diaz de la Guardia R. & Sanchez A. 2003: Sex chromosomes pairing in two Arvicolidae species: Microtys nivalis and Arvicola sapidus. - Hereditas 138: 114-121 Go to original source...
  28. Nguyen P., Sykorova M., Sichova J., Kuta V., Dalikova M., Capkova Frydrychova R., Neven L.G., Sahara K. & Marec F. 2013: Neo-sex chromosomes and adaptive potential in tortricid pests. - Proc. Natl. Acad. Sci. USA 110: 6931-6936 Go to original source...
  29. Palacios-Gimenez O.M., Castillo E.R., Marti D.A. & Cabral-de-Mello D.C. 2013: Tracking the evolution of sex chromosome system in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. - BMC Evol. Biol. 13: 167 Go to original source...
  30. Rebagliati P.J. & Mola L.M. 2010: Meiotic behaviour and karyotypic variation in Acledra (Pantatomidae, Heteroptera). - Genet. Mol. Res. 9: 739-749 Go to original source...
  31. Schweizer D. 1976: Reverse fluorescent chromosome banding with chromomycin and DAPI. - Chromosoma 58: 307-324 Go to original source...
  32. Sumner S.G. 1972: A simple technique for demonstrating centromere heterochromatin. - Exp. Cell. Res. 75: 304-306 Go to original source...
  33. Ueshima N. & Rentz D.C. 1979: Chromosome systems in the North American Decticinae with references to robertsonian changes (Orthoptera: Tettigoniidae). - Cytologia 44: 693-714 Go to original source...
  34. 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
  35. Warchalowska-Sliwa E. & Bugrov A.G. 1998: Karyotypes and C-banding patterns of some Phaneropterinae katydids (Orthoptera, Tettigonioidea) with special attention to a post-reductional division of the neo-X and the neo-Y sex chromosomes in Isophya hemiptera. - Folia Biol. (Krakow) 46: 47-54
  36. Warchalowska-Sliwa E. & Bugrov A.G. 2009: Karyotype of the South African katydid Hetrodes pupus (Linnaeus, 1758) (Orthoptera, Tettigoniidae) with special reference to relationships within the Hetrodinae subfamily. - Zootaxa 2137: 43-50
  37. 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...
  38. Warchalowska-Sliwa E., Grzywacz B., Maryanska-Nadachowska A., Karamysheva T.V., Rubtsov N.B. & Chobanov D.P. 2009: Chromosomal differentiation among bisexual European species of Saga Charp. (Orthoptera, Tettigoniidae, Saginae) detected by both classical and molecular methods. - Eur. J. Entomol. 106: 1-9 Go to original source...
  39. Warchalowska-Sliwa E., Maryanska-Nadachowska A., Grzywacz B., Karamysheva T., Lehmann A.W., Lehmann G.U.C. & Heller K.-G. 2011: Changes in the numbers of chromosomes and sex determination system in bushcrickets of the genus Odontura (Orthoptera, Tettigoniidae, Phaneropterinae). - Eur. J. Entomol. 108: 183-195 Go to original source...
  40. Warchalowska-Sliwa E., Grzywacz B., Maryanska-Nadachowska A., Karamysheva T., Heller K.-G., Lehmann A.W., Lehmann G.U.C. & Chobanov D.P. 2013a: Molecular and classical chromosomal techniques reveal diversity in bushcricket genera of Barbitistini (Orthoptera). - Genome 56: 667-676 Go to original source...
  41. Warchalowska-Sliwa E., Grzywacz B., Maryanska-Nadachowska A., Karamysheva T., Chobanov D.P. & Heller K.-G. 2013b: Cytogenetic variability among Bradyporinae species (Orthoptera: Tettigoniidae). - Eur. J. Entomol. 110: 1-12 Go to original source...
  42. Webber B.J., Rentz D.C., Ueshima N. & Woodrow I.E. 2003: Leucopodoptera eumundii, a new genus and species of katydid from the tropical rainforest of North Queensland, Australia (Orthoptera: Tettigoniidae: Phaneropterinae: Holochlorini). - J. Orthopt. Res. 12: 79-88 Go to original source...
  43. Weidner H. 1955: Die Hetrodinae (Orthoptera, Saltatoria). - Mitt. Hambg. Zool. Mus. Inst. 53: 109-172
  44. White M.J.D. 1973: Animal Cytology and Evolution. 3rd ed. Cambridge University Press, London, 961 pp
  45. White M.J.D. 1979: Karyotypes and meiosis of the morabine grasshoppers. II. The genera Culmacris and Stiletta. - Aust. J. Zool. 27: 109-133 Go to original source...
  46. White M.J.D., Blackith R.E., Blackith R.M. & Cheney J. 1967a: Cytogenetics of the viatica group of morabinae grasshoppers. I. The "coastal" species. - Aust. J. Zool. 15: 263-302 Go to original source...
  47. White M.J.D., Mesa A. & Mesa R. 1967b: Neo-XY sex chromosome mechanisms in two species of Tettigonioidea (Orthoptera). - Cytologia 32: 190-199 Go to original source...