Skip to main content
Log in

Resolution of sex chromosome constitution by genomic in situ hybridization and fluorescence in situ hybridization with (TTAGG) n telomeric probe in some species of Lepidoptera

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

We have developed a simple method to resolve the sex chromosome constitution in females of Lepidoptera by using a combination of genomic in situ hybridization (GISH) and fluorescence in situ hybridization with (TTAGG) n telomeric probe (telomere-FISH). In pachytene configurations of sex chromosomes, GISH differentiated W heterochromatin and telomere-FISH detected the chromosome ends. With this method we showed that Antheraea yamamai has a standard system with a fully differentiated W–Z sex chromosome pair. In Orgyia antiqua, we confirmed the presence of neo-W and neo-Z chromosomes, which most probably originated by fusion of the ancestral W and Z with an autosome pair. In contrast to earlier data, Orgyia thyellina females displayed a neo-ZW1W2 sex chromosome constitution. A neo-WZ1Z2 trivalent was found in females of Samia cynthia subsp. indet., originating from a population in Nagano, Japan. Whereas another subspecies collected in Sapporo, Japan, and determined as S. cynthia walkeri, showed a neo-W/neo-Z bivalent similar to O. antiqua, and the subspecies S. cynthia ricini showed a Z univalent (a Z/ZZ system). The combination of GISH and telomere-FISH enabled us to acquire not only reliable information about sex chromosome constitution but also an insight into sex chromosome evolution in Lepidoptera.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ayling LJ, Griffin DK (2002) The evolution of sex chromosomes. Cytogenet Genome Res 99:125–140

    Article  PubMed  Google Scholar 

  • Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308

    PubMed  CAS  Google Scholar 

  • Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130:113–146

    Article  Google Scholar 

  • Chowdhary BP, Raudsepp T, Frönicke L, Scherthan H (1998) Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo-FISH. Genome Res 8:577–589

    PubMed  CAS  Google Scholar 

  • Dedderer P (1928) Variations in chromosome number in the spermatogenesis of Philosamia cynthia. J Morphol Physiol 45:599–613

    Article  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2004) Viability of autosome translocations in mammals: an epigeomic hypothesis from a rodent case-study. Chromosoma 113:34–41

    Article  PubMed  CAS  Google Scholar 

  • Frydrychová R, Grossmann P, Trubac P, Vítková M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178

    Article  PubMed  Google Scholar 

  • Graves JAM (1998) Evolution of the mammalian Y chromosome and sex-determining genes. J Exp Zool 281:472–481

    Article  PubMed  CAS  Google Scholar 

  • Grützner F, Rens W, Tsend-Ayush E, El-Mogharbel N, O'Brien PCM, Jones RC, Ferguson-Smith MA, Graves JAM (2004) In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432:913–917

    Article  PubMed  CAS  Google Scholar 

  • Guan XY, Meltzer PS, Trent JM (1994) Rapid generation of whole chromosome painting probes (WCPs) by chromosome microdissection. Genomics 22:101–107

    Article  PubMed  CAS  Google Scholar 

  • Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG) n generated by PCR. Nucleic Acids Res 19:4780

    Article  PubMed  CAS  Google Scholar 

  • Jacobs DH (2004) The evolution of a neo-XY1Y2 sex chromosome system by autosome–sex chromosome fusion in Dundocoris nodulicarinus Jacobs (Heteroptera: Aradidae: Carventinae). Chromosome Res 12:175–191

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi E (1934) Zytologische Untersuchungen am Seidenspinner und seiner Verwandten. II. Spermatogenesese bei Antheraea yamamai Guérin, Antheraea pernyi Guénin, und ihre Bastard. Jap J Genet 10:135–151

    Google Scholar 

  • Kawaguchi E (1937) Chromosomenketten beim Rassenbastarde des Seidenspinners Philosamia cynthia. (Zytologische Untersuchungen am Seidenspinner und seinen Verwandten. III.) Cytologia Fujii II:(8)1023–1033

    Google Scholar 

  • Kirkpatrick M, Hall DW (2004) Sexual selection and sex linkage. Evolution 58:683–691

    PubMed  Google Scholar 

  • Kjellman C, Sjogren H-O, Widegren B (1995) The Y chromosome: a graveyard for endogenous retroviruses. Gene 73:86–91

    Google Scholar 

  • Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta). J Zoolog Syst Evol Res 38:73–79

    Article  Google Scholar 

  • Marec F (1996) Synaptonemal complex in insects. Int J Insect Morphol Embryol 25:205–233

    Article  Google Scholar 

  • Marec F, Novák K (1998) Absence of sex chromatin corresponds with a sex-chromosome univalent in females of Trichoptera. Eur J Entomol 95:197–209

    Google Scholar 

  • Marec F, Traut W (1994) Sex chromosome pairing and sex chromatin bodies in W–Z translocation strains of Ephestia kuehniella (Lepidoptera). Genome 37:426–435

    Google Scholar 

  • Marec F, Tothová A, Sahara K, Traut W (2001) Meiotic pairing of sex chromosome fragments and its relation to atypical transmission of a sex-linked marker in Ephestia kuehniella (Insecta: Lepidoptera). Heredity 87:659–671

    Article  PubMed  CAS  Google Scholar 

  • McAllister BF (2003) Sequence differentiation associated with an inversion on the neo-X chromosome of Drosophila americana. Genetics 165:1317–1328

    PubMed  CAS  Google Scholar 

  • Mediouni J, Fuková I, Frydrychová R, Dhouibi MH, Marec F (2004) Karyotype, sex chromatin and sex chromosome differentiation in the carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). Caryologia 57:184–194

    Google Scholar 

  • Nilsson N-O, Löfstedt C, Dävring L (1988) Unusual sex chromosome inheritance in six species of small ermine moths (Yponomeuta, Yponomeutidae, Lepidoptera). Hereditas 108:259–265

    Google Scholar 

  • Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fujiwara H (1993) Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol Cell Biol 13:1424–1432

    PubMed  CAS  Google Scholar 

  • Presgraves DC (2002) Patterns of postzygotic isolation in Lepidoptera. Evolution 56:1168–1183

    PubMed  Google Scholar 

  • Prowell DP (1998) Sex linkage and speciation in Lepidoptera. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 309–319

    Google Scholar 

  • Rasmussen SW, Holm PB (1982) The meiotic prophase in Bombyx mori. In King RC, Akai H (eds) Insect ultrastructure. Plenum, New York, pp 61–85

    Google Scholar 

  • Rego A, Marec F (2003) Telomeric and interstitial telomeric sequences in holokinetic chromosomes of Lepidoptera: telomeric DNA mediates association between postpachytene bivalents in achiasmatic meiosis of females. Chromosome Res 11:681–684

    Article  PubMed  CAS  Google Scholar 

  • Reinhold K (1998) Sex linkage among genes controlling sexually selected traits. Behav Ecol Sociobiol 44:1–7

    Article  Google Scholar 

  • Rens W, Grützner F, O'Brien PCM, Fairclough H, Graves JAM, Ferguson-Smith MA (2004) Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc Natl Acad Sci U S A 101:16257–16261

    Article  PubMed  CAS  Google Scholar 

  • Rishi S, Sahni G, Rishi KK (1999) Inheritance of unusual sex chromosome evidenced by AAWZ trivalent in Trabala vishnu (Lasiocampidae, Lepidoptera). Cytobios 100:85–94

    Google Scholar 

  • Robinson R (1971) Lepidoptera genetics. Pergamon, Oxford

    Google Scholar 

  • Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460

    Article  PubMed  CAS  Google Scholar 

  • Sahara K, Marec F, Eickhoff U, Traut W (2003a) Moth sex chromatin probed by comparative genomic hybridization (CGH). Genome 46:339–342

    Article  PubMed  CAS  Google Scholar 

  • Sahara K, Yoshido A, Kawamura N, Ohnuma A, Abe H, Mita K, Oshiki T, Shimada T, Asano S, Bando H, Yasukochi Y (2003b) W-derived BAC probes as a new tool for identification of the W chromosome and its aberrations in Bombyx mori. Chromosoma 112:48–55

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Feichtinger W, Steinlein C, Garcia RV, Badillo AF (2003) Chromosome banding in Amphibia. XXVIII. Homomorphic XY sex chromosomes and a derived Y-autosome translocation in Eleutherodactylus riveroi (Anura, Leptodactylidae). Cytogenet Genome Res 101:62–73

    Article  PubMed  CAS  Google Scholar 

  • Seiler J (1921) Geschlechtschromosomen-Untersuchung an Psychiden. II. Die Chromosomenzyklen von Fumea casta und Talaeporia tubulosa. Arch Zellforsch 16:18–46

    Google Scholar 

  • Seiler J (1925) Zytologische Vererbungsstudien an Schmetterlingen. I. Ergebnisse aus Kreuzungen von Schmetterlingsrassen mit verschiedner Chromosomenzahl. Arch Julius Klaus Stift Vererbungsforsch 1:63–117

    Google Scholar 

  • Shibata F, Hizume M, Kuroki Y (1999) Chromosome painting Y chromosomes and isolation of a Y chromosome specific repetitive sequence in the dioecious plant Rumex acetosa. Chromosoma 108:266–270

    Article  PubMed  CAS  Google Scholar 

  • Song F, Banno Y, Kawaguchi Y, Koga K, Xiang Z (1996) Dimorphism in chromosome number of Samia cynthia walkeri in China. Int J Wild Silkmoth Silk 2:11–13

    Google Scholar 

  • Steinemann M, Steinmann S, Lottspeich F (1993) How Y chromosomes become genetically inert. Proc Natl Acad Sci U S A 90:5737–5741

    Article  PubMed  CAS  Google Scholar 

  • Suomalainen E (1969a) On the sex chromosome trivalent in some Lepidoptera females. Chromosoma 28:298–308

    Article  Google Scholar 

  • Suomalainen E (1969b) Chromosome evolution in the Lepidoptera. Chromosomes Today 2:132–138

    Google Scholar 

  • Tanaka Y (1916) Genetic studies in the silkworm. J Coll Agr Sapporo 7:129–255

    Google Scholar 

  • Toder R, O'Neill RJ, Wienberg J, O'Brien PC, Voullaire L, Marshall-Graves JA (1997) Comparative chromosome painting between two marsupials: origins of an XX/XY1Y2 sex chromosome system. Mamm Genome 8:418–422

    Article  PubMed  CAS  Google Scholar 

  • Traut W (1999) The evolution of sex chromosomes in insects: differentiation of sex chromosomes in flies and moths. Eur J Entomol 96:227–235

    Google Scholar 

  • Traut W, Clarke CA (1996) Cytogenetics of a moth species with a low chromosome number, Orgyia thyellina. Hereditas 125:277–283

    Article  Google Scholar 

  • Traut W, Clarke CA (1997) Karyotype evolution by chromosome fusion in the moth genus Orgyia. Hereditas 126:77–84

    Article  Google Scholar 

  • Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71:239–256

    Article  PubMed  CAS  Google Scholar 

  • Traut W, Marec F (1997) Sex chromosome differentiation in some species of Lepidoptera (Insecta). Chromosome Res 5:283–291

    Article  PubMed  CAS  Google Scholar 

  • Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosome probed by comparative genomic hybridization. Chromosoma 108:173–180

    Article  PubMed  CAS  Google Scholar 

  • Ueno K, Ota K, Kobayashi T (2001) Heteromorphic sex chromosomes of lizardfish (Synodontidae): focus on the ZZ–ZW1W2 system in Trachinocephalus myops. Genetica 111:133–142

    Article  PubMed  CAS  Google Scholar 

  • Wahrman J, Richler C, Neufeld E, Friedmann A (1983) The origin of multiple sex chromosomes in the gerbil Gerbillus gerbillus (Rodentia: Gerbillinae). Cytogenet Cell Genet 35:161–180

    PubMed  CAS  Google Scholar 

  • Weiss-Schneeweiss H, Riha K, Jang CG, Puizina J, Scherthan H, Schweizer D (2004) Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesises vertebrate-type telomere sequence. Plant J 37:484–493

    Article  PubMed  CAS  Google Scholar 

  • Wolf KW (1996) The structure of condensed chromosomes in mitosis and meiosis of insects. Int J Insect Morphol Embryol 25:37–62

    Article  Google Scholar 

  • Yoshido A, Bando H, Yasukochi Y, Sahara K (2005) The Bombyx mori karyotype and assignment of linkage groups. Genetics (in press)

Download references

Acknowledgements

We thank Drs. Toru Shimada (Tokyo University, Tokyo, Japan) and Hitoshi Saito (Kyoto Institute of Technology, Kyoto, Japan) for providing broods of cynthia silk moths. Our thanks also go to Dr. Issei Ohshima (Hokkaido University, Sapporo, Japan) for identification of S. cynthia walkeri. K.S. was supported by grant-in-aid for scientific research 15380227 of the Japan Society for the Promotion of Science (JSPS) and from the Insect Technology Project 2013 of the Ministry of Agriculture, Forestry and Fisheries in Japan, Tokyo. F.M. was supported by grant A6007307 of the Grant Agency of the Academy of Sciences of the Czech Republic, Prague. Finally, we acknowledge the research fellowship given to F.M. from JSPS in 2003.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ken Sahara.

Additional information

Communicated by E.A. Nigg

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshido, A., Marec, F. & Sahara, K. Resolution of sex chromosome constitution by genomic in situ hybridization and fluorescence in situ hybridization with (TTAGG) n telomeric probe in some species of Lepidoptera. Chromosoma 114, 193–202 (2005). https://doi.org/10.1007/s00412-005-0013-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-005-0013-9

Keywords

Navigation