Large-scale comparative analysis of cytogenetic markers across Lepidoptera
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34108567
PubMed Central
PMC8190105
DOI
10.1038/s41598-021-91665-7
PII: 10.1038/s41598-021-91665-7
Knihovny.cz E-zdroje
- MeSH
- cytogenetické vyšetření metody MeSH
- genom MeSH
- hybridizace in situ fluorescenční MeSH
- mapování chromozomů MeSH
- molekulární evoluce * MeSH
- motýli genetika MeSH
- můry genetika MeSH
- ribozomální DNA genetika MeSH
- RNA malá jaderná genetika MeSH
- RNA ribozomální 18S genetika MeSH
- RNA ribozomální 5S genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
- RNA malá jaderná MeSH
- RNA ribozomální 18S MeSH
- RNA ribozomální 5S MeSH
- U2 small nuclear RNA MeSH Prohlížeč
Fluorescence in situ hybridization (FISH) allows identification of particular chromosomes and their rearrangements. Using FISH with signal enhancement via antibody amplification and enzymatically catalysed reporter deposition, we evaluated applicability of universal cytogenetic markers, namely 18S and 5S rDNA genes, U1 and U2 snRNA genes, and histone H3 genes, in the study of the karyotype evolution in moths and butterflies. Major rDNA underwent rather erratic evolution, which does not always reflect chromosomal changes. In contrast, the hybridization pattern of histone H3 genes was well conserved, reflecting the stable organisation of lepidopteran genomes. Unlike 5S rDNA and U1 and U2 snRNA genes which we failed to detect, except for 5S rDNA in a few representatives of early diverging lepidopteran lineages. To explain the negative FISH results, we used quantitative PCR and Southern hybridization to estimate the copy number and organization of the studied genes in selected species. The results suggested that their detection was hampered by long spacers between the genes and/or their scattered distribution. Our results question homology of 5S rDNA and U1 and U2 snRNA loci in comparative studies. We recommend the use of histone H3 in studies of karyotype evolution.
European Molecular Biology Laboratory Heidelberg Germany
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The Netherlands
Institute of Entomology Biology Centre CAS České Budějovice Czech Republic
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Traut W, Ahola V, Smith DAS, Gordon IJ, ffrench-Constant RH. Karyotypes versus genomes: The nymphalid butterflies Melitaeacinxia, Danausplexippus, and D.chrysippus. Cytogenet. Genome Res. 2017;153:46–53. doi: 10.1159/000484032. PubMed DOI
Heng HH, et al. A postgenomic perspective on molecular cytogenetics. CG. 2018;19:227–239. doi: 10.2174/1389202918666170717145716. PubMed DOI PMC
Deakin JE, et al. Chromosomics: Bridging the gap between genomes and chromosomes. Genes. 2019;10:627. doi: 10.3390/genes10080627. PubMed DOI PMC
Lewin HA, et al. Earth BioGenome Project: Sequencing life for the future of life. PNAS. 2018;115:4325–4333. doi: 10.1073/pnas.1720115115. PubMed DOI PMC
Claussen U. Chromosomics. Cytogenet. Genome Res. 2005;111:101–106. doi: 10.1159/000086377. PubMed DOI
Graphodatsky AS. Comparative chromosomics. Mol. Biol. 2007;41:361–375. doi: 10.1134/S002689330703003X. PubMed DOI
Dutrillaux B, Couturier J, Richer C-L, Viegas-Péquignot E. Sequence of DNA replication in 277 R- and Q-bands of human chromosomes using a BrdU treatment. Chromosoma. 1976;58:51–61. doi: 10.1007/BF00293440. PubMed DOI
Bickmore, W. A. Karyotype analysis and chromosome banding. In EncyclopediaofLifeSciences (ed. Wiley) a0001160 (Wiley, 2001).
King M. C-Banding studies on Australian hylid frogs: Secondary constriction structure and the concept of euchromatin transformation. Chromosoma. 1980;80:191–217. doi: 10.1007/BF00286300. DOI
Steiniger GE, Mukherjee AB. Insect chromosome banding: technique for G- and Q-banding pattern in the mosquito Aedesalbopictus. Can. J. Genet. Cytol. 1975;17:241–244. doi: 10.1139/g75-031. PubMed DOI
Brum-Zorrilla N, Postiglioni A. Banding pattern in chromosomes of Lycosa species (Araneae-Lycosidae) Genetica. 1980;54:149–153. doi: 10.1007/BF00055984. DOI
Cabrero J, Camacho JPM. Cytogenetic studies in gomphocerine grasshoppers. I. Comparative analysis of chromosome C-banding pattern. Heredity. 1986;56:365–372. doi: 10.1038/hdy.1986.58. DOI
Chen R, Song W, Li X, An Z. Chromosome G-banding in plants by inducing with trypsin and urea. Cell Res. 1994;4:79–87. doi: 10.1038/cr.1994.8. DOI
Song YC, et al. Comparisons of G-banding patterns in six species of the Poaceae. Hereditas. 2004;121:31–38. doi: 10.1111/j.1601-5223.1994.00031.x. DOI
Bedo DG. Karyotypic and chromosome banding studies of the potato tuber moth, Phthorimaeaoperculella (Zeller) (Lepidoptera, Gelechiidae) Can. J. Genet. Cytol. 1984;26:141–145. doi: 10.1139/g84-024. DOI
Prins, J. D. & Saitoh, K. Karyology and sex determination. In Band4:Arthropoda,2Hälfte:Insecta,Lepidoptera,MothsandButterflies,Teilband/Part36,Vol2:Morphology,Physiology,andDevelopment (ed. Kükenthal, W.) (DE GRUYTER, 2003).
Van Nieukerken EJ, et al. Order Lepidoptera Linnaeus, 1758. In: Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa. 2011;3148:212. doi: 10.11646/zootaxa.3148.1.41. PubMed DOI
Yoshido A, et al. Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies. Heredity. 2020;125:138–154. doi: 10.1038/s41437-020-0325-9. PubMed DOI PMC
Nguyen P, et al. Neo-sex chromosomes and adaptive potential in tortricid pests. PNAS. 2013;110:6931–6936. doi: 10.1073/pnas.1220372110. PubMed DOI PMC
Picq S, et al. Insights into the structure of the spruce budworm (Choristoneurafumiferana) genome, as revealed by molecular cytogenetic analyses and a high-density linkage map. G3. 2018;8:2539–2549. doi: 10.1534/g3.118.200263. PubMed DOI PMC
Asser-Kaiser S, et al. Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science. 2007;317:1916–1918. doi: 10.1126/science.1146542. PubMed DOI
Carabajal Paladino LZ, et al. Sex chromosome turnover in moths of the diverse superfamily Gelechioidea. Genome Biol. Evol. 2019;11:1307–1319. doi: 10.1093/gbe/evz075. PubMed DOI PMC
Labbé R, Caveney S, Donly C. Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol. Biol. 2010;20:243–256. doi: 10.1111/j.1365-2583.2010.01064.x. PubMed DOI
Wolf-I KW, Novák K, Marec F. Kinetic organization of metaphase I bivalents in spermatogenesis of Lepidoptera and Trichoptera species with small chromosome numbers. Heredity. 1997;79:35–143.
Fuková I, Nguyen P, Marec F. Codling moth cytogenetics: Karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome. 2005;48:1083–1092. doi: 10.1139/g05-063. PubMed DOI
Gan Y, et al. Individual chromosome identification, chromosomal collinearity and genetic-physical integrated map in Gossypiumdarwinii and four D genome cotton species revealed by BAC-FISH. Genes Genet. Syst. 2012;87:233–241. doi: 10.1266/ggs.87.233. PubMed DOI
Carabajal Paladino LZ, Nguyen P, Šíchová J, Marec F. Mapping of single-copy genes by TSA-FISH in the codling moth, Cydiapomonella. BMC Genet. 2014;15:S15. doi: 10.1186/1471-2156-15-S2-S15. PubMed DOI PMC
Traut W. Pachytene mapping in the female silkworm, Bombyxmori L. (Lepidoptera) Chromosoma. 1976;58:275–284. doi: 10.1007/BF00292094. PubMed DOI
Nguyen P, Sahara K, Yoshido A, Marec F. Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera) Genetica. 2010;138:343–354. doi: 10.1007/s10709-009-9424-5. PubMed DOI
Vershinina AO, Anokhin BA, Lukhtanov VA. Ribosomal DNA clusters and telomeric (TTAGG)n repeats in blue butterflies (Lepidoptera, Lycaenidae) with low and high chromosome numbers. CCG. 2015;9:161–171. doi: 10.3897/CompCytogen.v9i2.4715. PubMed DOI PMC
Yoshido A, Bando H, Yasukochi Y, Sahara K. The Bombyxmori karyotype and the assignment of linkage groups. Genetics. 2005;170:675–685. doi: 10.1534/genetics.104.040352. PubMed DOI PMC
Lukhtanov VA, et al. Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. PNAS. 2018;115:E9610–E9619. doi: 10.1073/pnas.1802610115. PubMed DOI PMC
Lee Y-I, et al. Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genom. 2018;19:578. doi: 10.1186/s12864-018-4956-7. PubMed DOI PMC
Cabral-de-Mello DC, Martins C, Souza MJ, Moura RC. Cytogenetic mapping of 5S and 18S rRNAs and H3 histone genes in 4 ancient Proscopiidae grasshopper species: Contribution to understanding the evolutionary dynamics of multigene families. Cytogenet. Genome Res. 2011;132:89–93. doi: 10.1159/000317476. PubMed DOI
García-Souto D, Troncoso T, Pérez M, Pasantes JJ. Molecular cytogenetic analysis of the European hake Merlucciusmerluccius (Merlucciidae, Gadiformes): U1 and U2 snRNA gene clusters map to the same location. PLoS One. 2015;10:e0146150. doi: 10.1371/journal.pone.0146150. PubMed DOI PMC
Kobayashi T, Heck DJ, Nomura M, Horiuchi T. Expansion and contraction of ribosomal DNA repeats in Saccharomycescerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev. 1998;12:3821–3830. doi: 10.1101/gad.12.24.3821. PubMed DOI PMC
Prokopowich CD, Gregory TR, Crease TJ. The correlation between rDNA copy number and genome size in eukaryotes. Genome. 2003;46:48–50. doi: 10.1139/g02-103. PubMed DOI
Cabral-de-Mello DC, Moura RC, Martins C. Chromosomal mapping of repetitive DNAs in the beetle Dichotomiusgeminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement. Heredity. 2010;104:393–400. doi: 10.1038/hdy.2009.126. PubMed DOI
Cabral-de-Mello DC, Oliveira SG, de Moura RC, Martins C. Chromosomal organization of the 18S and 5S rRNAs and histone H3 genes in Scarabaeinaecoleopterans: Insights into the evolutionary dynamics of multigene families and heterochromatin. BMC Genet. 2011;12:88. doi: 10.1186/1471-2156-12-88. PubMed DOI PMC
Badaeva ED, et al. A set of cytogenetic markers allows the precise identification of all A-genome chromosomes in diploid and polyploid wheat. Cytogenet. Genome Res. 2015;146:71–79. doi: 10.1159/000433458. PubMed DOI
Wang W, et al. Remarkable variation of ribosomal DNA organization and copy number in gnetophytes, a distinct lineage of gymnosperms. Ann. Bot. 2019;123:767–781. doi: 10.1093/aob/mcy172. PubMed DOI PMC
Palacios-Gimenez OM, Castillo ER, Martí DA, Cabral-de-Mello DC. Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol. Biol. 2013;13:167. doi: 10.1186/1471-2148-13-167. PubMed DOI PMC
Vierna J, Wehner S, Höner zu Siederdissen C, Martínez-Lage A, Marz M. Systematic analysis and evolution of 5S ribosomal DNA in metazoans. Heredity. 2013;111:410–421. doi: 10.1038/hdy.2013.63. PubMed DOI PMC
Garcia S, Garnatje T, Kovařík A. Plant rDNA database: Ribosomal DNA loci information goes online. Chromosoma. 2012;121:389–394. doi: 10.1007/s00412-012-0368-7. PubMed DOI
Sochorová J, Garcia S, Gálvez F, Symonová R, Kovařík A. Evolutionary trends in animal ribosomal DNA loci: Introduction to a new online database. Chromosoma. 2018;127:141–150. doi: 10.1007/s00412-017-0651-8. PubMed DOI PMC
Anjos A, et al. U1 snDNA clusters in grasshoppers: Chromosomal dynamics and genomic organization. Heredity. 2015;114:207–219. doi: 10.1038/hdy.2014.87. PubMed DOI PMC
Barzotti R, Pelliccia F, Rocchi A. Identifcation and characterization of U1 small nuclear RNA genes from two crustacean isopod species. Chromosome Res. 2003;11:365–373. doi: 10.1023/A:1024048108918. PubMed DOI
Cabral-de-Mello DC, Valente GT, Nakajima RT, Martins C. Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromisniloticus. Chromosome Res. 2012;20:279–292. doi: 10.1007/s10577-011-9271-y. PubMed DOI
Merlo MA, et al. Analysis of the histone cluster in Senegalese sole (Soleasenegalensis): Evidence for a divergent evolution of two canonical histone clusters. Genome. 2017;60:441–453. doi: 10.1139/gen-2016-0143. PubMed DOI
Piscor D, Fernandes CA, Parise-Maltempi PP. Conserved number of U2 snDNA sites in Piabinaargentea, Piabarchusstramineus and two Bryconamericus species (Characidae, Stevardiinae) Neotrop. Ichthyol. 2018;16:e170066. doi: 10.1590/1982-0224-20170066. DOI
Sember A, et al. Dynamics of tandemly repeated DNA sequences during evolution of diploid and tetraploid botiid loaches (Teleostei: Cobitoidea: Botiidae) PLoS One. 2018;13:e0195054. doi: 10.1371/journal.pone.0195054. PubMed DOI PMC
Poletto AB, et al. Chromosome differentiation patterns during cichlid fish evolution. BMC Genet. 2010;11:50. doi: 10.1186/1471-2156-11-50. PubMed DOI PMC
Symonová R, et al. Genome differentiation in a species pair of coregonine fishes: An extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol. Biol. 2013;13:42. doi: 10.1186/1471-2148-13-42. PubMed DOI PMC
de Sene VF, et al. Mapping of the retrotransposable elements Rex1 and Rex3 in chromosomes of Eigenmannia (Teleostei, Gymnotiformes, Sternopygidae) Cytogenet. Genome Res. 2015;146:319–324. doi: 10.1159/000441465. PubMed DOI
Cai Q, Zhang D, Liu Z-L, Wang X-R. Chromosomal localization of 5S and 18S rDNA in five species of subgenus Strobus and their implications for genome evolution of Pinus. Ann. Bot. 2006;97:715–722. doi: 10.1093/aob/mcl030. PubMed DOI PMC
Grozeva S, Kuznetsova V, Anokhin B. Karyotypes, male meiosis and comparative FISH mapping of 18S ribosomal DNA and telomeric (TTAGG)n repeat in eight species of true bugs (Hemiptera, Heteroptera) CCG. 2011;5:355–374. doi: 10.3897/compcytogen.v5i4.2307. PubMed DOI PMC
Chirino MG, Bressa MJ. Karyotype evolution in progress: A new diploid number in Belostomacandidulum (Heteroptera: Belostomatidae) from Argentina leading to new insights into its ecology and evolution. Eur. J. Entomol. 2014;111:165–174. doi: 10.14411/eje.2014.027. DOI
Roehrdanz R, Heilmann L, Senechal P, Sears S, Evenson P. Histone and ribosomal RNA repetitive gene clusters of the boll weevil are linked in a tandem array: Histone-ribosomal DNA repeats. Insect Mol. Biol. 2010;19:463–471. PubMed
Schienman JE, Lozovskaya ER, Strausbaugh LD. Drosophilavirilis has atypical kinds and arrangements of histone repeats. Chromosoma. 1998;107:529–539. doi: 10.1007/s004120050339. PubMed DOI
Zhang L, Bao Z, Wang S, Huang X, Hu J. Chromosome rearrangements in Pectinidae (Bivalvia: Pteriomorphia) implied based on chromosomal localization of histone H3 gene in four scallops. Genetica. 2007;130:193–198. doi: 10.1007/s10709-006-9006-8. PubMed DOI
Silva DMZA, et al. Chromosomal organization of repetitive DNA sequences in Astyanaxbockmanni (Teleostei, Characiformes): Dispersive location, association and co-localization in the genome. Genetica. 2013;141:329–336. doi: 10.1007/s10709-013-9732-7. PubMed DOI
Maxson R, Cohn R, Kedes L, Mohun T. Expression and organization of histone genes. Annu. Rev. Genet. 1983;17:239–277. doi: 10.1146/annurev.ge.17.120183.001323. PubMed DOI
Eirín-López JM, et al. Molecular evolutionary characterization of the mussel Mytilus histone multigene family: First record of a tandemly repeated unit of five histone genes containing an H1 subtype with ‘Orphon’ features. J. Mol. Evol. 2004;58:131–144. doi: 10.1007/s00239-003-2531-5. PubMed DOI
Šíchová J, Nguyen P, Dalíková M, Marec F. Chromosomal evolution in tortricid moths: Conserved karyotypes with diverged features. PLoS One. 2013;8:e64520. doi: 10.1371/journal.pone.0064520. PubMed DOI PMC
Šíchová J, et al. Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evol. Biol. 2015;15:89. doi: 10.1186/s12862-015-0375-4. PubMed DOI PMC
Mutanen M, Wahlberg N, Kaila L. Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proc. R. Soc. B. 2010;277:2839–2848. doi: 10.1098/rspb.2010.0392. PubMed DOI PMC
Wiemers M, Chazot N, Wheat C, Schweiger O, Wahlberg N. A complete time-calibrated multi-gene phylogeny of the European butterflies. ZooKeys. 2020;938:97–124. doi: 10.3897/zookeys.938.50878. PubMed DOI PMC
Kawahara AY, et al. Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. PNAS. 2019;116:22657–22663. doi: 10.1073/pnas.1907847116. PubMed DOI PMC
Marec F, Traut W. Synaptonemal complexes in female and male meiotic prophase of Ephestiakuehniella (Lepidoptera) Heredity. 1993;71:394–404. doi: 10.1038/hdy.1993.154. DOI
Zrzavá M, et al. Sex chromosomes of the iconic moth Abraxasgrossulariata (Lepidoptera, Geometridae) and its congener A.sylvata. Genes. 2018;9:279. doi: 10.3390/genes9060279. PubMed DOI PMC
Kiauta B, Lankhorst L. The chromosomes of the caddis-fly, Glyphotaeliuspellucidus (Retzius, 1783) (Trichoptera: Limnephilidae, Limnephilinae) Genetica. 1969;40:1–6. doi: 10.1007/BF01787334. PubMed DOI
Lukhtanov VA. Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta) J. Zool. Syst. Evol. Res. 2000;38:73–79. doi: 10.1046/j.1439-0469.2000.382130.x. DOI
Seiler J. Research on the sex-chromosomes of Psychidae (Lepidoptera) Biol. Bull. 1919;36:399–404. doi: 10.2307/1536220. DOI
Seiler J. Geschlechtschromosomen-Untersuchungen an Psychiden. Z. Indukt. Abstamm. Vererbungsl. 1922;31:1–99.
Hejníčková M, et al. Absence of W chromosome in Psychidae moths and implications for the theory of sex chromosome evolution in Lepidoptera. Genes. 2019;10:1016. doi: 10.3390/genes10121016. PubMed DOI PMC
Dalíková M, et al. New insights into the evolution of the W chromosome in Lepidoptera. J. Hered. 2017;108:709–719. doi: 10.1093/jhered/esx063. PubMed DOI
Prins JD, Prins WD, Dall’Asta U. The karyotype of Camerariaohridella (Lepidoptera: Gracillariidae) Phegea. 2002;301:5–10.
Kawazoé A. The chromosome in the primitive or microlepidopterous moth-groups II. Proc. Jpn. Acad. Ser. B. 1987;63:87–90. doi: 10.2183/pjab.63.87. DOI
Nilsson N-O, Löfstedt C, Dävring L. Unusual sex chromosome inheritance in six species of small ermine moths (Yponomeuta, Yponomeutidae, Lepidoptera) Hereditas. 1988;108:259–265. doi: 10.1111/j.1601-5223.1988.tb00311.x. DOI
Ortiz E, Templado J. Los cromosomas de tres especies de tortrícidos (Lep. Tortricidae) EOS Rev. Esp. Entomol. 1976;51:77–84.
Robinson, R. LepidopteraGenetics. (Pergamon Press, 1971).
Carabajal Paladino LZ, et al. The effect of X-rays on cytological traits of Tutaabsoluta (Lepidoptera: Gelechiidae) Fla. Entomol. 2016;99:43–53. doi: 10.1653/024.099.sp107. DOI
Schulz H-J, Traut W. The pachytene complement of the wildtype and a chromosome mutant strain of the flour moth, Ephestiakuehniella (Lepidoptera) Genetica. 1979;50:61–66. doi: 10.1007/BF00122679. DOI
Van’t Hof AE, et al. Linkage map of the peppered moth, Bistonbetularia (Lepidoptera, Geometridae): A model of industrial melanism. Heredity. 2013;110:283–295. doi: 10.1038/hdy.2012.84. PubMed DOI PMC
Kawamura N. Cytological studies on the mosaic silkworms induced by low temperature treatment. Chromosoma. 1979;74:179–188. doi: 10.1007/BF00292271. DOI
Bytinski-Salz, H. Untersuchungen an Lepidopteren-hybriden V. Die Verwandfschaft der Platysamia-Arten (Lepidoptera, Saturniidae) nach Untersuchungen über die Fertilität und die Chromosomenverhältnisse ihrer Bastarde. Arch. Exp. Zellforsch22, 217–237 (1938).
Ahola V, et al. The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera. Nat. Commun. 2014;5:4737. doi: 10.1038/ncomms5737. PubMed DOI PMC
da Silva M, Ribeiro ED, Matoso DA. Chromosomal polymorphism in two species of Hypancistrus (Siluriformes: Loricariidae): An integrative approach for understanding their biodiversity. Genetica. 2014;142:127–139. PubMed
Supiwong W, et al. Karyotype diversity and evolutionary trends in the Asian swamp eel Monopterusalbus (Synbranchiformes, Synbranchidae): A case of chromosomal speciation? BMC Evol. Biol. 2019;19:73. doi: 10.1186/s12862-019-1393-4. PubMed DOI PMC
Šíchová J, et al. Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptideaamurensis. Biol. J. Linn. Soc. 2016;118:457–471. doi: 10.1111/bij.12756. DOI
Lukhtanov VA, Dincă V, Talavera G, Vila R. Unprecedented within-species chromosome number cline in the Wood White butterfly Leptideasinapis and its significance for karyotype evolution and speciation. BMC Evol. Biol. 2011;11:109. doi: 10.1186/1471-2148-11-109. PubMed DOI PMC
Hill J, et al. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Sci. Adv. 2019;5:eaau3648. doi: 10.1126/sciadv.aau3648. PubMed DOI PMC
Ferguson L, et al. Ancient expansion of the Hox cluster in Lepidoptera generated four Homeobox genes implicated in extra-embryonic tissue formation. PLoS Genet. 2014;10:e1004698. doi: 10.1371/journal.pgen.1004698. PubMed DOI PMC
Thomas GWC, et al. Gene content evolution in the arthropods. Genome Biol. 2020;21:15. doi: 10.1186/s13059-019-1925-7. PubMed DOI PMC
Cheng R-L, Yu Y-X, Liu L-X, Zhang C-X, Fang C-X. A draft genome of the ghost moth, Thitarodes (Hepialus) sp., a medicinal caterpillar fungus. Insect Sci. 2016;23:326–329. doi: 10.1111/1744-7917.12292. PubMed DOI
Fraïsse C, Picard MAL, Vicoso B. The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W. Nat. Commun. 2017;8:1486. doi: 10.1038/s41467-017-01663-5. PubMed DOI PMC
Aguilera PM, Debat HJ, Scaldaferro MA, Martí DA, Grabiele M. FISH-mapping of the 5S rDNA locus in chili peppers (Capsicum-Solanaceae) An. Acad. Bras. Ciênc. 2016;88:117–125. doi: 10.1590/0001-37652301620140616. PubMed DOI
Volkov RA, et al. Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid Atropa belladonna. BMC Plant. Biol. 2017;17:21. doi: 10.1186/s12870-017-0978-6. PubMed DOI PMC
Mount SM, Gotea V, Lin C-F, Hernandez K, Makalowski W. Spliceosomal small nuclear RNA genes in 11 insect genomes. RNA. 2006;13:5–14. doi: 10.1261/rna.259207. PubMed DOI PMC
Marz M, Kirsten T, Stadler PF. Evolution of spliceosomal snRNA genes in metazoan animals. J. Mol. Evol. 2008;67:594–607. doi: 10.1007/s00239-008-9149-6. PubMed DOI
Mesa A, Somarelli JA, Herrera RJ. Small nuclear RNA variants of three Bombyxmori strains. Entomol. Res. 2008;38:61–68. doi: 10.1111/j.1748-5967.2008.00131.x. DOI
Merlo MA, Cross I, Rodríguez-Rúa A, Manchado M, Rebordinos L. First approach to studying the genetics of the meagre (Argyrosomus regius; Asso, 1801) using three multigene families. Aquac. Res. 2013;44:974–984. doi: 10.1111/j.1365-2109.2012.03103.x. DOI
Mediouni J, Fuková I, Frydrychová R, Dhouibi MH, Marec F. Karyotype, sex chromatin and sex chromosome differentiation in the carob moth, Ectomyeloisceratoniae (Lepidoptera: Pyralidae) Caryologia. 2004;57:184–194. doi: 10.1080/00087114.2004.10589391. DOI
Lockwood A. “Ringer” solutions and some notes on the physiological basis of their ionic composition. Comp. Biol. Phys. 1961;2:241–289. PubMed
Rovatsos M, Altmanová M, Pokorná M, Kratochvíl L. Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution. 2014;68:2079–2085. doi: 10.1111/evo.12357. PubMed DOI
Blin N, Stafford DW. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976;3:2303–2308. doi: 10.1093/nar/3.9.2303. PubMed DOI PMC
Ferguson KB, et al. Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest. Insect Mol. Biol. 2020;30:188–209. doi: 10.1111/imb.12688. PubMed DOI PMC
Fuková I, et al. Probing the W chromosome of the codling moth, Cydiapomonella, with sequences from microdissected sex chromatin. Chromosoma. 2007;116:135–145. doi: 10.1007/s00412-006-0086-0. PubMed DOI