Abstract
We examined chromosomal distribution of major ribosomal DNAs (rDNAs), clustered in the nucleolar organizer regions (NORs), in 18 species of moths and butterflies using fluorescence in situ hybridization with a codling moth (Cydia pomonella) 18S rDNA probe. Most species showed one or two rDNA clusters in their haploid karyotype but exceptions with 4–11 clusters also occurred. Our results in a compilation with previous data revealed dynamic evolution of rDNA distribution in Lepidoptera except Noctuoidea, which showed a highly uniform rDNA pattern. In karyotypes with one NOR, interstitial location of rDNA prevailed, whereas two-NOR karyotypes showed mostly terminally located rDNA clusters. A possible origin of the single interstitial NOR by fusion between two NOR-chromosomes with terminal rDNA clusters lacks support in available data. In some species, spreading of rDNA to new, mostly terminal chromosome regions was found. The multiplication of rDNA clusters without alteration of chromosome numbers rules out chromosome fissions as a major mechanism of rDNA expansion. Based on rDNA dynamics in Lepidoptera and considering the role of ordered nuclear architecture in karyotype evolution, we propose ectopic recombination, i.e., homologous recombination between repetitive sequences of non-homologous chromosomes, as a primary motive force in rDNA repatterning.
Similar content being viewed by others
References
Adams SP, Leitch IJ, Bennet MD, Chase MW, Leitch AR (2000) Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). Am J Bot 87:1578–1583
Aylon Y, Kupiec M (2004) DSB repair: the yeast paradigm. DNA Repair 3:797–815
Bartlett AC, Del Fosse FE (1991) The pachytene karyotype of the pink bollworm (Lepidoptera: Gelechiidae). Southwest Entomol 16:223–235
Bedo DG (1984) Karyotypic and chromosome banding studies of the potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera, Gelechiidae). Can J Genet Cytol 26:141–145
Beldade P, Saenko SV, Pul N, Long AD (2009) A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome. PLoS Genet 5:e1000366
Bigger TRL (1975) Karyotypes of some Lepidoptera chromosomes and changes in their holokinetic organisation as revealed by new cytological techniques. Cytologia 40:713–726
Bombarová M, Marec F, Nguyen P, Špakulová M (2007) Divergent location of ribosomal genes in chromosomes of fish thorny-headed worms, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). Genetica 131:141–149
Brown KS, Freitas AVL, Wahlberg N, von Schoultz B, Saura AO, Saura A (2007) Chromosomal evolution in the South American Nymphalidae. Hereditas 144:137–148
Cabrero J, Camacho JPM (2008) Location and expression of ribosomal RNA genes in grasshoppers: abundance of silent and cryptic loci. Chromosome Res 16:595–607
Choo KH, Vissel B, Brown R, Filby RG, Earle E (1988) Homologous alpha satellite sequences on human acrocentric chromosomes with selectivity for chromosomes 13, 14 and 21: implications for recombination between nonhomologues and Robertsonian translocations. Nucleic Acids Res 16:1273–1284
Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S (2006) Chromosome territories—a functional nuclear landscape. Curr Opin Cell Biol 18:307–316
Datson PM, Murray BG (2006) Ribosomal DNA locus evolution in Nemesia: transposition rather than structural rearrangement as the key mechanism? Chromosome Res 14:845–857
Dubcovsky J, Dvořák J (1995) Ribosomal-RNA multigene loci: nomads of the Triticeae genomes. Genetics 140:1367–1377
Emelianov I, Marec F, Mallet J (2004) Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc R Soc Lond B 271:97–105
Fuková I, Nguyen P, Marec F (2005) Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48:1083–1092
Fuková I, Traut W, Vítková M, Nguyen P, Kubíčková S, Marec F (2007) Probing the W chromosome of the codling moth, Cydia pomonella, with sequences from microdissected sex chromatin. Chromosoma 116:135–145
Goldman ASH, Lichten M (1996) The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144:43–55
Grimaldi D, Engel MS (2005) Evolution of the Insects. Cambridge University Press, New York
Hall KJ, Parker JS (1995) Stable chromosome fission associated with rDNA mobility. Chromosome Res 3:417–422
Hanson RE, Islam-Faridi MN, Percival EA, Crane CF, Ji YF, McKnight TD, Stelly DM, Price HJ (1996) Distribution of 5S and 18S–28S rDNA loci in a tetraploid cotton (Gossypium hirsutum L.) and its putative diploid ancestors. Chromosoma 105:55–61
Hirai H, Yamamoto MT, Taylor RW, Imai HT (1996) Genomic dispersion of 28S rDNA during karyotypic evolution in the ant genus Myrmecia (Formicidae). Chromosoma 105:190–196
Kandul NP, Lukhtanov VA, Pierce NE (2007) Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution 61:546–559
Keil CB, Mason CE, Showers WB (1990) Apyrene spermatogenesis in Ostrinia nubilalis (Hübner): obligate and facultative diapausing strains. J Hered 81:72–74
Krider HM, Shields KS (1997) Meiosis in North American and Asian races of gypsy moth (Lepidoptera: Lymantriidae) and their hybrids. Ann Entomol Soc Am 90:223–229
Kristensen NP (ed) (1999) Lepidoptera, Moths and Butterflies, vol 1: Evolution, Systematics, and Biogeography. Handbook of Zoology, vol IV, Arthropoda: Insecta, part 35. Walter de Gruyter, Berlin, New York
Kundu SC, Ibotombi N, Bhagirath T (1991) Synaptonemal complex karyotype of an Indian silkworm, Antheraea roylei. Sericologia 31:545–547
Lewis LC, Lynch RE (1969) Rearing the European corn borer, Ostrinia nubilalis (Hübner), on diets containing corn leaf and wheat germ. Iowa State J Sci 44:9–14
Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta). J Zoolog Syst Evol Res 38:73–79
Maggini F, Cremonini R, Zolfino C, Tucci GF, D′Ovidio R, Delre V, DePace C, Scarascia Mugnozza GT, Cionini PG (1991) Structure and chromosomal localization of DNA sequences related to ribosomal subrepeats in Vicia faba. Chromosoma 100:229–234
Mahendran B, Ghosh SK, Kundu SC (2006) Molecular phylogeny of silk-producing insects based on 16S ribosomal RNA and cytochrome oxidase subunit I genes. J Genet 85:31–38
Marec F, Traut W (1993) Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera). Heredity 71:394–404
Marshall WF (2002) Order and disorder in the nucleus. Curr Biol 12:R185–R192
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
Mieczkowski PA, Lemoine FJ, Petes TD (2006) Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 5:1010–1020
Mitchell A, Mitter C, Regier JC (2006) Systematics and evolution of the cutworm moths (Lepidoptera: Noctuidae): evidence from two protein-coding nuclear genes. Syst Entomol 31:21–46
Monti L, Lemeunier F, Lalanne-Cassou B (1998) A chromosomal investigation of two closely related species of Spodoptera. Compt Rendus Acad Sci III Sci Vie 321:275–282
Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152
Pedrosa-Harand A, de Almeida CCS, Mosiolek M, Blair M, Schweizer D, Guerra M (2006) Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet 112:924–933
Pringle EG, Baxter SW, Webster CL, Papanicolaou A, Lee SF, Jiggins CD (2007) Synteny and chromosome evolution in the Lepidoptera: evidence from mapping in Heliconius melpomene. Genetics 177:417–426
Raskina O, Belyayev A, Nevo E (2004) Activity of the En/Spm-like transposons in meiosis as a base for chromosome repatterning in a small, isolated, peripheral population of Aegilops speltoides Tausch. Chromosome Res 12:153–161
Regier JC, Cook CP, Mitter C, Hussey A (2008) A phylogenetic study of the “bombycoid complex” (Lepidoptera) using five protein-coding nuclear genes, with comments on the problem of macrolepidopteran phylogeny. Syst Entomol 33:175–189
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 11:681–694
Robinson R (1971) Lepidoptera Genetics. Pergamon Press, Oxford
Roy V, Monti-Dedieu L, Chaminade N, Siljak-Yakovlev S, Aulard S, Lemeunier F, Montchamp-Moreau C (2005) Evolution of the chromosomal location of rDNA genes in two Drosophila species subgroups: ananassae and melanogaster. Heredity 94:388–395
Sahara K, Yoshido A, Kawamura N, Ohnuma A, Abe H, Mita K, Oshiki T, Shimada T, Asano S, Bando H, Yasukochi Y (2003) W-derived BAC probes as a new tool for identification of the W chromosome and its aberrations in Bombyx mori. Chromosoma 112:48–55
Sahara K, Yoshido A, Marec F, Fuková I, Zhang HB, Wu CC, Goldsmith MR, Yasukochi Y (2007) Conserved synteny of genes between chromosome 15 of Bombyx mori and a chromosome of Manduca sexta shown by five-color BAC-FISH. Genome 50:1061–1065
Schlecht HB, Lichten M, Goldman ASH (2004) Compartmentalization of the yeast meiotic nucleus revealed by analysis of ectopic recombination. Genetics 168:1189–1203
Schubert I (1984) Mobile nucleolus organizing regions (NORs) in Allium (Liliaceae s. lat.)? Inferences from the specifity of silver staining. Plant Syst Evol 144:291–305
Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148
Shalev G, Levy AA (1997) The maize transposable element Ac induces recombination between the donor site and an homologous ectopic sequence. Genetics 146:1143–1151
Shishido R, Sano Y, Fukui K (2000) Ribosomal DNAs: an exception to the conservation of gene order in rice genomes. Mol Gen Genet 263:586–591
Song M, Boissinot S (2007) Selection against LINE-1 retrotransposons results principally from their ability to mediate ectopic recombination. Gene 390:206–213
Stahl A, Luciani JM, Hartung M, Devictor M, Bergé-Lefranc JL, Guichaoua M (1983) Structural basis for Robertsonian translocations in man: association of ribosomal genes in the nucleolar fibrillar center in meiotic spermatocytes and oocytes. Proc Natl Acad Sci USA 80:5946–5950
Suomalainen E (1966) Achiasmatische Oogenese bei Trichopteren. Chromosoma 18:201–207
Traut W (1976) Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284
Traut W, Clarke CA (1996) Cytogenetics of a moth species with a low chromosome number, Orgyia thyellina. Hereditas 125:277–283
Traut W, Clarke CA (1997) Karyotype evolution by chromosome fusion in the moth genus Orgyia. Hereditas 126:77–84
Traut W, Marec F (1997) Sex chromosome differentiation in some species of Lepidoptera (Insecta). Chromosome Res 5:283–291
Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108:173–180
Traut W, Sahara K, Marec F (2007) Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1:332–346
Van’t Hof AE, Marec F, Saccheri IJ, Brakefield PM, Zwaan BJ (2008) Cytogenetic characterization and AFLP-based genetic linkage mapping for the butterfly Bicyclus anynana, covering all 28 karyotyped chromosomes. PLoS ONE 3:e3882
Vítková M, Fuková I, Kubíčková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15:917–930
Wahlberg N, Braby MF, Brower AV, de Jong R, Lee MM, Nylin S, Pierce NE, Sperling FA, Vila R, Warren AD, Zakharov E (2005) Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers. Proc Biol Sci 272:1577–1586
Wolf KW (1996) The structure of condensed chromosomes in mitosis and meiosis of insects. Int J Insect Morphol Embryol 25:37–62
Wolf KW, Novák K, Marec F (1997) Kinetic organization of metaphase I bivalents in spermatogenesis of Lepidoptera and Trichoptera species with small chromosome numbers. Heredity 79:135–143
Wrensch DL, Kethley JB, Norton RA (1994) Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalization on eukaryotes. In: Houck MA (ed) Mites: Ecological and Evolutionary Analyses of Life-History Patterns. Chapman & Hall, New York, pp 282–343
Yasukochi Y, Ashakumary LA, Baba K, Yoshido A, Sahara K (2006) A second-generation integrated map of the silkworm reveals synteny and conserved gene order between lepidopteran insects. Genetics 173:1319–1328
Yoshido A, Bando H, Yasukochi Y, Sahara K (2005a) The Bombyx mori karyotype and the assignment of linkage groups. Genetics 170:675–685
Yoshido A, Marec F, Sahara K (2005b) 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
Yoshido A, Yamada Y, Sahara K (2006) The W chromosome detection in several lepidopteran species by genomic in situ hybridization (GISH). J Insect Biotech Sericol 75:147–151
Zhang D, Sang T (1999) Physical mapping of ribosomal RNA genes in peonies (Paeonia, Paeoniaceae) by fluorescent in situ hybridization: implications for phylogeny and concerted evolution. Am J Bot 86:735–740
Acknowledgments
We wish to thank Marie Korchová for technical assistance and our colleagues, Oxana Habuštová for Ostrinia nubilalis, Jiří Beneš, Zdeněk Fric, Josef Jaroš, and Martin Konvička for their help with collecting and determination of some species. Our thanks are also due to Zenta Kajiura (Shinshu University, Japan) for Antheraea pernyi through NBRP, Sandra Barns and Stuart Reynolds (Bath University, UK) for Manduca sexta, Josef Chytil (Přerov, Czech Republic) for Lymantria dispar, Tomáš Hamřík (Velká Bíteš, Czech Republic) for Arctia caja, and Zdeněk Hanč (České Budějovice) for valuable advice. This work was funded by grants 206/06/1860 of the Grant Agency of the Czech Republic (GACR) and IAA600960925 of the Grant Agency of the Academy of Sciences of the Czech Republic, both Prague, and from the Entomology Institute project Z50070508. P. N. acknowledges the support from the grant SGA2006/01 of the Student Grant Agency of the Faculty of Science, University of South Bohemia, Czech Republic, and the support of his Ph.D. programme by the GACR grant 521/08/H042. K. S. and A. Y. were supported from grants 18380037 and 191114 of the Japan Society for the Promotion of Science (JSPS), respectively.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nguyen, P., Sahara, K., Yoshido, A. et al. Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica 138, 343–354 (2010). https://doi.org/10.1007/s10709-009-9424-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-009-9424-5