Eur. J. Entomol. 117: 474-480, 2020 | DOI: 10.14411/eje.2020.050

Cytogenetic characterization of periodical cicadas (Hemiptera: Cicadidae: Magicicada)Original article

Gayane KARAGYAN1, Natalia GOLUB2, Teiji SOTA3
1 Scientific Center of Zoology and Hydroecology, NAS RA, P. Sevak 7, Yerevan, 0014 Armenia; e-mail: gaykaragyan@yahoo.com
2 Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034 St. Petersburg, Russia; e-mail: nvgolub@mail.ru
3 Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto, 606-8502 Japan; e-mail: sota@terra.zool.kyoto-u.ac.jp

The periodical cicadas of the genus Magicicada Davis, 1925 inhabiting eastern United States are characterized by a long juvenile period of 17 or 13 years and periodical mass emergence of adults. In this genus, only seven species are distinguished and are distributed into three species groups, Decim, Cassini and Decula. We performed comparative cytogenetic study of all seven Magicicada species, and 6 of them were explored for the first time. The techniques used included standard chromosome staining, differential chromosome staining techniques (C-banding, AgNOR-banding and fluorochrome DAPI-staining) and FISH (fluorescence in situ hybridization) with 18S rDNA and (TTAGG)n-telomeric probes. All these species have holokinetic chromosomes, like other Hemiptera. Karyotypes of all species appeared to be remarkably conserved with 2n = 19/20 (18 + X0/XX) (male/female); one very large pair of autosomes and all other chromosomes constituting a decreasing size series; X chromosomes were indistinguishable, at least, at mitotic metaphases. The nucleolus organizer regions (NORs) revealed on one of the medium-sized chromosome pairs in all species and were shown to coincide with the rDNA clusters revealed by FISH. In all species, very small blocks of C-heterochromatin were variously located on chromosomes clearly using DAPI but less distinctly by C-banding. The chromosomes of all the species studied were confirmed to contain the "insect type" motif of telomeres (TTAGG)n.

Keywords: Hemiptera, Cicadidae, Magicicada, periodical cicadas, chromosome numbers, karyotype, C-heterochromatin, nucleolus organizer regions, AT-rich regions, 18S rDNA, telomeres

Received: October 23, 2020; Revised: November 30, 2020; Accepted: November 30, 2020; Published online: December 15, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
KARAGYAN, G., GOLUB, N., & SOTA, T. (2020). Cytogenetic characterization of periodical cicadas (Hemiptera: Cicadidae: Magicicada). EJE, 117, Article 474-480. https://doi.org/10.14411/eje.2020.050
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Alexander R.D. & Moore T.E. 1962: The evolutionary relationships of 17-year and 13-year cicadas, and three new species (Homoptera, Cicadidae, Magicicada). - Misc. Publ. Mus. Zool. Univ. Mich. 121: 1-59.
    2. Anjos A., Rocha G.C., Paladini A., Mariguela T.C. & Cabral-de-Mello D.C. 2016: Karyotypes and repetitive DNA evolution in six species of the genus Mahanarva (Auchenorrhyncha: Cercopidae). - Cytogenet. Genome Res. 149: 321-327. Go to original source...
    3. Anokhin B., Hemmrich-Stanisak G. & Bosch T.C.G. 2010: Karyotyping and single-gene detection using fluorescence in situ hybridization on chromosomes of Hydra magnipapillata. - Comp. Cytogen. 4: 97-110. Go to original source...
    4. Chatterjee K. & Ghosh M. 1978: Chromosomes of four species of Himalayan cicadas. - Chromosome Inform. Serv. 24: 7-8.
    5. Conger A.D. & Fairchild L.M. 1953: A quick-freeze method for making smear slides permanent. - Stain Technol. 28: 281-283. Go to original source...
    6. Cooley J.R., Simon C., Marshall D.C., Slon K. & Ehrhardt C. 2001: Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera: Magicicada spp.): genetic, morphological, and behavioural evidence. - Mol. Ecol. 10: 661-671. Go to original source...
    7. Du Z., Hasegawa H., Cooley J.R., Simon C., Yoshimura J., Cai W., Sota T. & Li H. 2019: Mitochondrial genomics reveals shared phylogeographic patterns and demographic history among three periodical cicada species groups. - Mol. Biol. Evol. 36: 1187-1200. Go to original source...
    8. 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...
    9. Fujisawa T., Koyama T., Kakishima S., Cooley J.R., Simon C., Yoshimura J. & Sota T. 2018: Triplicate parallel life cycle divergence despite gene flow in periodical cicadas. - Commun. Biol. 1: 26, 14 pp. Go to original source...
    10. Golub N.V., Kuznetsova V.G. & Rakitov R.A. 2014: First karyotype data on the family Myerslopiidae (Hemiptera, Auchenorrhyncha, Cicadomorpha). - Comp. Cytogen. 8: 293-300. Go to original source...
    11. Golub N., Anokhin B. & Kuznetsova V. 2019: Comparative FISH mapping of ribosomal DNA clusters and TTAGG telomeric sequences to holokinetic chromosomes of eight species of the insect order Psocoptera. - Comp. Cytogen. 13: 403-410. Go to original source...
    12. Grozeva S., Kuznetsova V.G. & Anokhin B.A. 2010: Bed bug cytogenetics: karyotype, sex chromosome system, FISH mapping of 18S rDNA, and male meiosis in Cimex lectularius Linnaeus, 1758 (Heteroptera: Cimicidae). - Comp. Cytogen. 4: 151-160. Go to original source...
    13. Grozeva S., Anokhin B. & Kuznetsova V.G. 2015: Bed bugs (Hemiptera). In Sharakhov I. (ed.): Protocols for Cytogenetic Mapping of Arthropod Genomes. CRC Press, Taylor & Francis, Boca Raton, pp. 285-326. Go to original source...
    14. Howell W.M. & Black D.A. 1980: Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-srep method. - Experientia 36: 1014-1015. Go to original source...
    15. Karagyan G., Lachowska D. & Kalashian M. 2012: Karyotype analysis of four jewel-beetle species (Coleoptera, Buprestidae) detected by standard staining, C-banding, AgNOR-banding and CMA3/DAPI staining. - Comp. Cytogen. 6: 183-197. Go to original source...
    16. Kirillova V.I. 1986: Chromosome numbers of the leafhoppers (Homoptera, Auchenorrhyncha) of the world fauna. I. Superfamilies Fulgoroidea, Cercopoidea and Cicadoidea. - Entomol. Obozr. 65(1): 115-125 [in Russian; English transl. in Entomol. Rev. 65(4): 34-47].
    17. Kurokawa H.A. 1953: A studies of the chromosomes in some species of the Cicadidae and the Cercopidae. - Jap. J. Genet. 28: 1-5. Go to original source...
    18. Kuznetsova V. & Aguin-Pombo D. 2015: Comparative cytogenetics of Auchenorrhyncha (Hemiptera, Homoptera): a review. - ZooKeys 538: 63-93. Go to original source...
    19. Kuznetsova V.G., Grozeva S., Nokkala S. & Nokkala C. 2011: Cytogenetics of the true bug infraorder Cimicomorpha (Hemiptera: Heteroptera): a review. - ZooKeys 154: 31-70. Go to original source...
    20. Kuznetsova V.G., Maryańska-Nadachowska A., Anokhin B. & Aguin-Pombo D. 2015: Evidence for TTAGG telomere repeats and rRNA gene clusters in leafhoppers of the genus Alebra (Hemiptera: Auchenorrhyncha: Cicadellidae). - Eur. J. Entomol. 112: 207-214. Go to original source...
    21. Marshall D.C. & Cooley J.R. 2000: Reproductive character displacement and speciation in periodical cicadas, and a new 13-year species, Magicicada neotredecim. - Evolution 54: 1313-1325. Go to original source...
    22. Maryańska-Nadachowska A., Kuznetsova V.G. & Karamysheva T.V. 2013: Chromosomal location of rDNA clusters and TTAGG telomeric repeats in eight species of the spittlebug genus Philaenus (Hemiptera: Auchenorrhyncha: Aphrophoridae). - Eur. J. Entomol. 110: 411-418. Go to original source...
    23. Perepelov E., Bugrov A.G. & Maryańska-Nadachowska A. 2002: Constitutive heterochromatin in karyotypes of two Cicadidae species from Japan (Cicadoidea, Hemiptera). - Folia Biol. (Kraków) 50: 2017-2019.
    24. Rożek M. 2000: The C-banding technique for Coleoptera (Insecta). - Folia Biol. (Kraków) 48: 29-31.
    25. Sahara K., Marec F. & Traut W. 1999: TTAGG telomeric repeats in chromosomes of some insects and other arthropods. - Chromosom Res. 7: 449-460. Go to original source...
    26. Shaffer E.L. 1920: The germ cells of Cicada (Tibicen) septendecim (Homoptera). - Biol. Bull. 38: 404-474. Go to original source...
    27. Sota T., Yamamoto S., Cooley J.R., Hill K.B.R., Simon C. & Yoshimura J. 2013: Independent divergence of 13- and 17-y life cycles among three periodical cicada lineages. - PNAS 110: 6919-6924. Go to original source...
    28. Whitten M.I. 1965: Chromosome numbers in some Australian leaf-hoppers (Homoptera, Auchenorrhyncha). - Proc. Linn. Soc. N. S. W. 90: 78-85.
    29. Wilcox E.V. 1895: Spermatogenesis of Caloptenus femur-rubrim and Cicada tibicen. - Bull. Mus. Comp. Zool. Harv. Colleg. 27(1): 1-32.
    30. Williams K.S. & Simon C. 1995: The ecology, behavior, and evolution of periodical cicadas. - Annu. Rev. Entomol. 40: 269-295. Go to original source...

    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.


    Return to the content