Eur. J. Entomol. 112 (4): 599-605, 2015 | 10.14411/eje.2015.093

First chromosomal study of Mantophasmatodea: Karyotype of Karoophasma biedouwense (Austrophasmatidae)

Dorota LACHOWSKA-CIERLIK1, Anna MARYAŃSKA-NADACHOWSKA2, Valentina KUZNETSOVA3, Mike PICKER4
1 Institute of Zoology, Jagiellonian University, Cracow, Poland; e-mail: dorota.lachowska-cierlik@uj.edu.pl
2 Institute of Systematic and Evolution of Animals, PAS, Cracow, Poland; e-mail: maryanska@isez.pan.krakow.pl
3 Zoological Institute Russian Academy of Sciences, St. Petersburg, Russia; e-mail: valentina_kuznetsova@yahoo.com
4 Department of Biological Sciences, University of Cape Town, Rondebosch, Cape Town, South Africa; e-mail: mike.picker@uct.ac.za

We have investigated for the first time the chromosomes of Karoophasma biedouwense, a species belonging to the Mantophasmatodea, a recently discovered order of carnivorous insects. Our study has revealed that males of this species display testes with numerous seminal tubes (follicles), as in other Polyneoptera, and short tubular seminal vesicles embedded in a utricular gland. The karyotype consists of 2n = 12A + X monocentric and biarmed, meta/submetacentric chromosomes (fundamental number of arms: FN = 26) with blocks of heterochromatin around centromeres. The autosomes are classified into two size groups, one represented by a single, very large pair of autosomes, the other by five smaller pairs which constitute a continuous series gradually decreasing in size. Among "monocentric" orders of Polyneoptera, K. biedouwense shares its low chromosome number, 2n = 13, as also found with some Orthoptera (Acridoidea, Grylloidea, Gryllacridoidea). Male meiosis is of the classical pre-reductional type and the X(0) sex determination system is probably an ancestral state. Use of FISH along with an 18S rDNA probe revealed multiple ribosomal clusters, which most likely represent an apomorphic condition. We identified the ancestral insect telomeric sequence (TTAGG)n in the terminal areas of the chromosomes. Currently available data on the polyneopteran orders putatively related to Mantophasmatodea showed a wide variability of cytogenetic characteristics within and between them. The only character allowing some tentative inference to be made on the ancestry of K. biedouwense is its low chromosome number, the karyotypic pattern so far unreported for the Polyneoptera except in certain Orthoptera.

Keywords: Mantophasmatodea, Karoophasma biedouwense, FISH, heterochromatin, heelwalkers, meiosis, ribosomal genes, sex determination system, telomeres

Received: April 20, 2015; Accepted: July 3, 2015; Prepublished online: September 22, 2015; Published: November 21, 2015

Download citation

References

  1. Angus R.B. 2010: Boreonectes gen. n., a new genus for the Stictotarsus griseistriatus (De Geer) group of sibling species (Coleoptera: Dytiscidae) with additional karyosystematic data on the group. - Compar. Cytogen. 4: 123-131. Go to original source...
  2. Arillo A. & Engel M.S. 2006: Rock crawlers in Baltic amber (Notoptera: Mantophasmatodea). - Am. Mus. Nov. 3539: 1-10. Go to original source...
  3. Baccetti B. 1982: The spermatozoon of Arthropoda. XXXII. Galiosiana nipponensis (Caudel et King) (Grylloblattodea). In Ando H. (ed.): Biology of the Notoptera. Kashiyo-Insatsu, Nagano, pp. 71-78.
  4. Bergamaschi S., Dawes-Gromadzki T., Scali V., Marini M. & Mantovani B. 2007: Karyology, mitochondrial DNA and the phylogeny of Australian termites. - Chromos. Res. 15: 735-753. Go to original source...
  5. Blackman R.L. 1995: Sex Determination in Insects. Insect Reproduction. CRC Press, Boca Raton, FL, 255 pp.
  6. Buder G. & Klass K.D. 2013: The morphology of tarsal processes in Mantophasmatodea. - Dt. Entomol. Z. 60: 5-23.
  7. Cabral-de-Mello D.C., Cabrero J., López-León M.D. & Camacho J.P.M. 2011: Evolutionary dynamics of 5S rDNA location in acridid grasshoppers and its relationship with H3 histone gene and 45S rDNA location. - Genetica 139: 921-931. Go to original source...
  8. Cabrero J. & Camacho J.P.M. 2008: Location and expression of ribosomal RNA genes in grasshoppers: Abundance of silent and cryptic loci. - Chromos. Res. 16: 595-607. Go to original source...
  9. Cameron S.L., Barker S.C. & Whiting M.F. 2006: Mitochondrial geneomics and the new insect order Mantophasmatodea. - Mol. Phylogenet. Evol. 38: 274-279. Go to original source...
  10. del Cerro A.L., Cuñado N. & Santos J.L. 1998: Synaptonemal complex analysis of the X1X2Y trivalent in Mantis religiosa L. males: inferences on the origin and maintenance of the sex-determining mechanism. - Chromos. Res. 6: 5-11. Go to original source...
  11. Dallai R., Frati F., Lupetti P. & Adis J. 2003: Sperm ultrastructure of Mantophasma zephyra (Insecta: Mantophasmatodea). - Zoomorphology 122: 67-76.
  12. Donlon T.A. & Magenis R.E. 1983: Methyl green is a substitute for distamycin A in the formation of distamycin A/DAPI C-bands. - Human Genet. 65: 144-146. Go to original source...
  13. Frydrychová R., Grossmann P., Trubač P., Vítková M. & Marec F. 2004: Phylogenetic distribution of TTAGG telomeric repeats in insects. - Genome 47: 163-178. Go to original source...
  14. Golub N.V., Kuznetsova V.G. & Rakitov R.A. 2014: First karyotype data on the family Myerslopiidae (Hemiptera, Auchenorrhyncha, Cicadomorpha). - Compar. Cytogen. 8: 293-300.
  15. Gorochov A.V. 2004: Primitive Titanoptera and early evolution of Polyneoptera. - Meetings in Memory of N.A. Cholodkovsky 57(1): 1-54 [in Russian].
  16. Grozeva S., Anokhin B. & Kuznetsova V.G. 2014: Bed bugs (Hemiptera). In Sharachov I. (ed.): Protocols for Cytogenetic Mapping of Arthropod Genomes. CRC press, Taylor & Francis, Boca Raton, pp. 285-326.
  17. Grzywacz B., Maryańska-Nadachowska A., Chobanov D.P., Karamaysheva T. & Warchałowska-Śliwa E. 2011: Comparative analysis of the location of rDNA in the Palaearctic bushcricket genus Isophya (Orthoptera: Tettigoniidae: Phaneropterinae). - Eur. J. Entomol. 108: 509-517. Go to original source...
  18. Hewitt G.M. 1979: Animal Cytogenetics. Orthoptera - Grasshoppers and Crickets. Vol. 3: Insecta 1. Gebrüder Borntraeger, Berlin, Stuttgart, 170 pp.
  19. Hockman D., Picker M.D., Klass K.D. & Pretorius L. 2009: Postembryonic development of the unique antenna of Mantophasmatodea (Insecta). - Arthropod Struct. Devel. 38: 125-133. Go to original source...
  20. Hodson A.M., Cook S.E., Edgerly J.S. & Miller K.B. 2014: Parthenogenetic and sexual species within the Haploembia solieri species complex (Embioptera: Oligotomidae) found in California. - Insect Syst. Evol. 45: 93-113. Go to original source...
  21. Huang D., Nel A. & Zompro O. 2008: Mantophasmatodea now in the Jurassic. - Naturwissenschaften 95: 947-952. Go to original source...
  22. King M. 1993: Species Evolution - The Role of Chromosome Change. Cambridge University Press, Cambridge, 366 pp.
  23. Klass K.D. 2007: Die Stammesgeschichte der Hexapoden: eine kritische Diskussion neuerer Daten und Hypothesen. - Denisia 20: 413-450.
  24. Klass K.D., Zompro O., Kristensen N.P & Adis J. 2002: Mantophasmatodea: a new insect order with extant members in the afrotropics. - Science 296: 1456-1459. Go to original source...
  25. Klass K.D., Picker M.D., Damgaard J., Van Noort S. & Tojo K. 2003: The taxonomy, genitalic morphology, and phylogenetic relationships of South African Mantophasmatodea (Insecta). - Entomol. Abh. 61: 3-67.
  26. Kuznetsova V., Nokkala S. & Shcherbakov D. 2002: Karyotype, reproductive organs, and pattern of gametogenesis in Zorotypus hubbardi Caudell (Insecta: Zoraptera, Zorotypidae), with discussion on relationships of the order. - Can. J. Zool. 80: 1047-1054. Go to original source...
  27. Lachowska D., Rożek M. & Holecova M. 2009: Chromosomal similarities and differences among three sibling species of the Acalles echinatus group (Coleoptera, Curculionidae, Cryptorhynchinae). - Zootaxa 1985: 63-68.
  28. Lukhtanov V.A. & Kuznetsova V.G. 2010: What genes and chromosomes say about the origin and evolution of insects and other arthropods. - Russ. J. Genet. 46: 1115-1121. Go to original source...
  29. Lukhtanov V.A., Shapoval N.A. & Dantchenko A.V. 2008: Agrodiaetus shahkuhensis sp. n. (Lepidoptera, Lycaenidae), a cryptic species from Iran discovered by using molecular and chromosomal markers. - Compar. Cytogen. 2: 99-114.
  30. Maekawa K. & Nalepa C.A. 2011: Biogeography and phylogeny of wood-feeding cockroaches in the genus Cryptocercus. - Insects Sci. 2: 354-368. Go to original source...
  31. Maryańska-Nadachowska A., Kuznetsova V.G., Lachowska D. & Drosopoulos S. 2012: Mediterranean species of the spittlebug genus Philaenus: modes of chromosome evolution. - J. Insect Sci. 12: 1-17. Go to original source...
  32. Matsuda R. 1976: Morphology and Evolution of the Insect Abdomen (With Special Reference to Developmental Patterns and their Bearings upon Systematics). International Series in Pure and Applied Biology (Zoology Division). Vol. 56. Pergamon Press, Oxford, New York, Toronto, Sydney, Paris, Frankfurt, 534 pp.
  33. Myers S.S, Trewick S.A. & Morgan-Richards M. 2013: Multiple lines of evidence suggest mosaic polyploidy in the hybrid parthenogenetic stick insect lineage Acanthoxyla. - Insect Conserv. Divers. 6: 537-548. Go to original source...
  34. Nakamura K. & Kidata J.I. 1955: Chromosomes of some orthopteroid insects, with reference to sex-chromosomes. - Cytologia 20: 119-132. Go to original source...
  35. Picker M.D., Colville J.F. & Van Noort S. 2002: Mantophasmatodea now in South Africa. - Science 297: 1475. Go to original source...
  36. Plazzi F., Ricci A. & Passamonti M. 2011: The mitochondrial genome of Bacillus stick insects (Phasmatodea) and the phylogeny of orthopteroid insects. - Mol. Phylogenet. Evol. 58: 304-316. Go to original source...
  37. Predel R., Neuperts S., Huetteroth W., Kahnt J., Waidelich D. & Roth S. 2012: Peptidomics-based phylogeny and biogeography of Mantophasmatodea (Hexapoda). - Syst. Biol. 61: 609-629. Go to original source...
  38. Roth S., Molina J. & Predel R. 2014: Biodiversity, ecology, and behaviour of the recently discovered insect order Mantophasmatodea. - Front. Zool. 11: 70. Go to original source...
  39. Saez F.A. & Pérez-Mosquera G. 1977: Structure, behaviour and evolution of the chromosomes of Dichroplus silveiraguidoi (Orthoptera: Acrididae). - Genetica 47: 105-113. Go to original source...
  40. Scali V., Milani L. & Passamonti M. 2012: Revision of the stick insect genus Leptynia: description of new taxa, speciation mechanism and phylogeography. - Contr. Zool. 81: 25-42.
  41. Schweizer D. 1976: Reverse fluorescent chromosome banding with chromomycin and DAPI. - Chromosoma 58: 307-324. Go to original source...
  42. Sumner A.T. 1972: A simple technique for demonstrating centromeric heterochromatin. - Exp. Cell Res. 75: 304-306. Go to original source...
  43. Terry M.D. & Whiting M.F. 2005: Mantophasmatodea and phylogeny of the lower neopterous insects. - Cladistics 21: 240-257. Go to original source...
  44. Vítková M., Král J., Traut W., Zrzavý J. & Marec F. 2005: The evolutionary origin of insect telomeric repeats (TTAGGn). - Chromos. Res. 3: 145-156. Go to original source...
  45. Wang Y., Engel M.S., Rafael J.K., Dang K., Wu H., Wang Y., Xie Q. & Bu W. 2013: A unique box in 28S rRNA is shared by the enigmatic insect order Zoraptera and Dictyoptera. - PLoS One 8(1): e53679. Go to original source...
  46. Warchałowska-Śliwa E. 1998: Karyotype characteristics of katydid orthopterans (Ensifera, Tettigoniidae) and remarks on their evolution at different taxonomic levels. - Folia Biol. (Kraków) 46: 143-176.
  47. Warchałowska-Śliwa E., Grzywacz B., Maryańska-Nadachowska A., Karamysheva T., Chobanov D.P. & Heller K.G. 2013: Cytogenetic variability among Bradyporinae species (Orthoptera: Tettigoniidae). - Eur. J. Entomol. 110: 1-12. Go to original source...
  48. White M. 1976: Animal Cytogenetics. Vol. 3: Insecta 2. Gebrüder Borntraeger, Berlin, Stuttgart, 75 pp.
  49. Wipfler B., Bai M., Schoville S., Dallai R., Uchifune T., Machida R., Cui Y. & Beutel R.G. 2014: Ice crawlers (Grylloblattodea) - the history of the investigation of a highly unusual group of insects. - J. Insect Biodiv. 2: 1-25. Go to original source...
  50. Wipfler B., Klug R., Ge S.-Q., Bai M., Göbbels J., Yang X.-K. & Hörnschemeyer T. 2015: The thorax of Mantophasmatodea, the morphology of flightlessness and the evolution of the neopteran insects. - Cladistics 21: 50-70. Go to original source...
  51. Zompro O. 2001: The Phasmatodea and Raptophasma n. gen., Orthopetra incertae sedis in Baltic amber (Insecta: Orthoptera). - Mitt. Geol.-Paläontol. Inst. Univ. Hamburg 85: 229-261.
  52. Zompro O. 2005: Inter- and intra-ordinal relationships of the Mantophasmatodea, with comments on the phylogeny of polyneopteran orders (Insecta: Polyneoptera). - Mitt. Geol.-Paläontol. Inst. Univ. Hamburg 89: 85-116.