{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:10:41Z","timestamp":1790835041086,"version":"4.1.0"},"reference-count":95,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,8]],"date-time":"2023-02-08T00:00:00Z","timestamp":1675814400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["19-14-00202"],"award-info":[{"award-number":["19-14-00202"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Butterfly chromosomes are holocentric, i.e., lacking a localized centromere. Potentially, this can lead to rapid karyotypic evolution through chromosome fissions and fusions, since fragmented chromosomes retain kinetic activity, while fused chromosomes are not dicentric. However, the actual mechanisms of butterfly genome evolution are poorly understood. Here, we analyzed chromosome-scale genome assemblies to identify structural rearrangements between karyotypes of satyrine butterfly species. For the species pair Erebia ligea\u2013Maniola jurtina, sharing the ancestral diploid karyotype 2n = 56 + ZW, we demonstrate a high level of chromosomal macrosynteny and nine inversions separating these species. We show that the formation of a karyotype with a low number of chromosomes (2n = 36 + ZW) in Erebia aethiops was based on ten fusions, including one autosome\u2013sex chromosome fusion, resulting in a neo-Z chromosome. We also detected inversions on the Z sex chromosome that were differentially fixed between the species. We conclude that chromosomal evolution is dynamic in the satyrines, even in the lineage that preserves the ancestral chromosome number. We hypothesize that the exceptional role of Z chromosomes in speciation may be further enhanced by inversions and sex chromosome\u2013autosome fusions. We argue that not only fusions\/fissions but also inversions are drivers of the holocentromere-mediated mode of chromosomal speciation.<\/jats:p>","DOI":"10.3390\/genes14020437","type":"journal-article","created":{"date-parts":[[2023,2,9]],"date-time":"2023-02-09T02:32:07Z","timestamp":1675909927000},"page":"437","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Whole-Genome Analysis Reveals the Dynamic Evolution of Holocentric Chromosomes in Satyrine Butterflies"],"prefix":"10.3390","volume":"14","author":[{"given":"Elena A.","family":"Pazhenkova","sequence":"first","affiliation":[{"name":"Department of Biology, Biotechnical Faculty, University of Ljubljana, Ve\u010dna pot 111, 1000 Ljubljana, Slovenia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2856-2075","authenticated-orcid":false,"given":"Vladimir A.","family":"Lukhtanov","sequence":"additional","affiliation":[{"name":"Department of Karyosystematics, Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1508\/cytologia.6.422","article-title":"Notes on the mitotic behavior of long chromosomes","volume":"6","author":"Schrader","year":"1935","journal-title":"Cytologia"},{"key":"ref_2","unstructured":"White, M.J.D. (1973). Animal Cytology and Evolution, Cambridge University Press. [3rd ed.]."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Mandrioli, M., and Manicardi, G.C. (2020). Holocentric chromosomes. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1008918"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3153","DOI":"10.1016\/j.cell.2022.06.045","article-title":"Repeat-based holocentromeres influence genome architecture and karyotype evolution","volume":"185","author":"Hofstatter","year":"2022","journal-title":"Cell"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1007\/s10577-012-9292-1","article-title":"Holocentric chromosomes: Convergent evolution, meiotic adaptations, and genomic analysis","volume":"20","author":"Melters","year":"2012","journal-title":"Chromosome Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"evaa220","DOI":"10.1093\/gbe\/evaa220","article-title":"The evolution of chromosome numbers: Mechanistic models and experimental approaches","volume":"13","author":"Mayrose","year":"2022","journal-title":"Genome Biol. Evol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/s00412-015-0524-y","article-title":"Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution","volume":"124","author":"Jankowska","year":"2015","journal-title":"Chromosoma"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1093\/genetics\/106.2.185","article-title":"Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae","volume":"106","author":"Haber","year":"1983","journal-title":"Genetics"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s00412-004-0278-4","article-title":"Inverted meiosis and meiotic drive in mealybugs","volume":"112","author":"Bongiorni","year":"2004","journal-title":"Chromosoma"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5070","DOI":"10.1038\/ncomms6070","article-title":"Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes","volume":"5","author":"Cabral","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"4979","DOI":"10.1038\/ncomms5979","article-title":"Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans","volume":"5","author":"Heckmann","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1111\/brv.12096","article-title":"The cytogenetic architecture of the aphid genome","volume":"90","author":"Manicardi","year":"2015","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"515","DOI":"10.3897\/CompCytogen.v12i4.30431","article-title":"New data on karyotypes of lace bugs (Tingidae, Cimicomorpha, Hemiptera) with analysis of the 18S rDNA clusters distribution","volume":"12","author":"Golub","year":"2018","journal-title":"Comp. Cytogenet."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1093\/biolinnean\/blaa077","article-title":"Karyotype evolution and flexible (conventional versus inverted) meiosis in insects with holocentric chromosomes: A case study based on Polyommatus butterflies","volume":"130","author":"Lukhtanov","year":"2020","journal-title":"Biol. J. Linn. Soc."},{"key":"ref_15","first-page":"541","article-title":"Inverted meiosis and its place in the evolution of sexual reproduction pathways","volume":"52","author":"Bogdanov","year":"2016","journal-title":"Genetika"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"20160001","DOI":"10.1098\/rstb.2016.0001","article-title":"Evolutionary mysteries in meiosis","volume":"371","author":"Lenormand","year":"2016","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1146\/annurev-genet-120215-035100","article-title":"Conservation and variability of meiosis across the eukaryotes","volume":"50","author":"Loidl","year":"2016","journal-title":"Ann. Rev. Genet."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1111\/jeb.13580","article-title":"Inverted meiosis and the evolution of sex by loss of complementation","volume":"33","author":"Archetti","year":"2020","journal-title":"J. Evol. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"E9610","DOI":"10.1073\/pnas.1802610115","article-title":"Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids","volume":"115","author":"Lukhtanov","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"583827","DOI":"10.3389\/fgene.2020.583827","article-title":"Incomplete sterility of chromosomal hybrids: Implications for karyotype evolution and homoploid hybrid speciation","volume":"11","author":"Lukhtanov","year":"2020","journal-title":"Front. Genet."},{"key":"ref_21","first-page":"187","article-title":"Holocentric chromosomes","volume":"Volume 2","author":"Greilhuber","year":"2013","journal-title":"Plant Genome Diversity"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ruckman, S.N., Jonika, M.M., Casola, C., and Blackmon, H. (2020). Chromosome number evolves at equal rates in holocentric and monocentric clades. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1009076"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1093\/sysbio\/syab038","article-title":"DNA barcodes combined with multilocus data of representative taxa can generate reliable higher-level phylogenies","volume":"71","author":"Talavera","year":"2022","journal-title":"Syst. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/nature03704","article-title":"Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies","volume":"436","author":"Lukhtanov","year":"2005","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.ympev.2013.08.004","article-title":"In the shadow of phylogenetic uncertainty: The recent diversification of Lysandra butterflies through chromosomal change","volume":"69","author":"Talavera","year":"2013","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"683","DOI":"10.3897\/CompCytogen.v9i4.5760","article-title":"The blue butterfly Polyommatus (Plebicula) atlanticus (Lepidoptera, Lycaenidae) holds the record of the highest number of chromosomes in the non-polyploid eukaryotic organisms","volume":"9","author":"Lukhtanov","year":"2015","journal-title":"Comp. Cytogenet."},{"key":"ref_27","first-page":"1","article-title":"Sp\u00e9ciation et variation chromosomique chez les L\u00e9pidopt\u00e8res Rhopaloc\u00e8res","volume":"2","year":"1960","journal-title":"Annls Sci. Nat. Zool. S\u00e9r."},{"key":"ref_28","unstructured":"Robinson, R. (1971). Lepidoptera Genetics, Pergamon Press."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1111\/j.1601-5223.2004.01868.x","article-title":"Chromosome evolution in Neotropical Danainae and Ithomiinae (Lepidoptera)","volume":"141","author":"Brown","year":"2004","journal-title":"Hereditas"},{"key":"ref_30","first-page":"369","article-title":"Die Chromosomenkomplexe und ihre Beziehung zur Phylogenie bei den Lepidopteren","volume":"14","author":"Beliajeff","year":"1930","journal-title":"Z. F\u00fcr Inductive Abstamm. Und Verer."},{"key":"ref_31","first-page":"132","article-title":"Chromosome evolution in Lepidoptera","volume":"2","author":"Suomalainen","year":"1969","journal-title":"Chromosome Today"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1046\/j.1439-0469.2000.382130.x","article-title":"Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta)","volume":"38","author":"Lukhtanov","year":"2000","journal-title":"J. Zool. Syst. Evol. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4737","DOI":"10.1038\/ncomms5737","article-title":"The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera","volume":"5","author":"Ahola","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"\u0160\u00edchov\u00e1, J., Volen\u00edkov\u00e1, A., Dinc\u0103, V., Nguyen, P., Vila, R., Sahara, K., and Marec, F. (2015). Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evol. Biol., 15.","DOI":"10.1186\/s12862-015-0375-4"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1111\/bij.12756","article-title":"Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis","volume":"118","author":"Ohno","year":"2016","journal-title":"Biol. J. Linn. Soc. Lond."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1139\/G07-082","article-title":"Conserved synteny of genes between chromosome 15 of Bombyx mori and a chromosome of Manduca sexta shown by five-color BAC-FISH","volume":"50","author":"Sahara","year":"2007","journal-title":"Genome"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.ibmb.2013.04.003","article-title":"FISH identification of Helicoverpa armigera and Mamestra brassicae chromosomes by BAC and fosmid probes","volume":"43","author":"Sahara","year":"2013","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"eaau3648","DOI":"10.1126\/sciadv.aau3648","article-title":"Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution","volume":"5","author":"Hill","year":"2019","journal-title":"Sci. Adv."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4449","DOI":"10.1093\/molbev\/msab185","article-title":"Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci but consistently depends on chromosome size","volume":"38","author":"Cicconardi","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"jkac069","DOI":"10.1093\/g3journal\/jkac069","article-title":"The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome","volume":"12","author":"Mackintosh","year":"2022","journal-title":"G3-Genes Genom. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1007\/s10577-023-09713-z","article-title":"High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptidea spp.)","volume":"31","author":"Vila","year":"2023","journal-title":"Chromosome Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1534\/genetics.107.073122","article-title":"Synteny and chromosome evolution in the Lepidoptera: Evidence from mapping in Heliconius melpomene","volume":"177","author":"Pringle","year":"2007","journal-title":"Genetics"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Papa, R., Morrison, C.M., Walters, J.R., Counterman, B.A., Chen, R., Halder, G., Ferguson, L., Chamberlain, N., Ffrench-Constant, R., and Kapan, D.D. (2008). Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-345"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Beldade, P., Saenko, S.V., Pul, N., and Long, A.D. (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.","DOI":"10.1371\/journal.pgen.1000366"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"7680","DOI":"10.1073\/pnas.0910413107","article-title":"Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements","volume":"107","author":"Sezutsu","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1534\/g3.115.023655","article-title":"Major improvements to the Heliconius melpomene genome assembly used to confirm 10 chromosome fusion events in 6 million years of butterfly evolution","volume":"6","author":"Davey","year":"2016","journal-title":"G3-Genes Genom. Genet."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Yasukochi, Y., Tanaka-Okuyama, M., Shibata, F., Yoshido, A., Marec, F., Wu, C., Zhang, H., Goldsmith, M.R., and Sahara, K. (2009). Extensive conserved synteny of genes between the karyotypes of Manduca sexta and Bombyx mori revealed by BAC-FISH mapping. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0007465"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"jkac047","DOI":"10.1093\/g3journal\/jkac047","article-title":"Population differentiation and structural variation in the Manduca sexta genome across the United States","volume":"12","author":"Mongue","year":"2022","journal-title":"G3-Genes Genom. Genet."},{"key":"ref_49","first-page":"72","article-title":"Caract\u00e8res et repartition en France d\u2019Erebia aethiopellus Hoffmsg. et E. mnestra Hb","volume":"1","year":"1959","journal-title":"Alexanor"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"The Darwin Tree of Life Project Consortium (2022). Sequence locally, think globally: The Darwin tree of life project. Proc. Natl. Acad. Sci. USA, 119, e2115642118.","DOI":"10.1073\/pnas.2115642118"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"296","DOI":"10.12688\/wellcomeopenres.17304.1","article-title":"The genome sequence of the meadow brown, Maniola jurtina (Linnaeus, 1758)","volume":"6","author":"Lohse","year":"2021","journal-title":"Wellcome Open. Res."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"259","DOI":"10.12688\/wellcomeopenres.18115.1","article-title":"The genome sequence of the Arran brown, Erebia ligea (Linnaeus, 1758) [version 1; peer review: Awaiting peer review]","volume":"7","author":"Lohse","year":"2022","journal-title":"Wellcome Open. Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"217","DOI":"10.12688\/wellcomeopenres.17927.1","article-title":"The genome sequence of the scotch argus butterfly, Erebia aethiops (Esper, 1777)","volume":"7","author":"Lohse","year":"2022","journal-title":"Wellcome Open. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: Pairwise alignment for nucleotide sequences","volume":"34","author":"Li","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Winter, D., Lee, K., and Cox, M. (2022, December 18). 2020 pafr: Read, Manipulate and Visualize Pairwise mApping Format. Available online: https:\/\/dwinter.github.io\/pafr\/.","DOI":"10.32614\/CRAN.package.pafr"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e251","DOI":"10.7717\/peerj-cs.251","article-title":"RIdeogram: Drawing SVG graphics to visualize and map genome-wide data on the idiograms","volume":"6","author":"Hao","year":"2020","journal-title":"PeerJ Comput. Sci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An information aesthetic for comparative genomics","volume":"19","author":"Krzywinski","year":"2009","journal-title":"Genome Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2811","DOI":"10.1093\/bioinformatics\/btu393","article-title":"circlize implements and enhances circular visualization in R","volume":"30","author":"Gu","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1111\/j.1601-5223.1938.tb03219.x","article-title":"Chromosomenzahlen finnl\u00e4ndischer Lepidopteren I. Rhopalocera","volume":"24","author":"Federley","year":"1938","journal-title":"Hereditas"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/BF00325958","article-title":"Die Chromosomezahlen in der Spermatogenese der Tagfalter","volume":"2","year":"1941","journal-title":"Chromosoma"},{"key":"ref_61","first-page":"149","article-title":"Chromosome numbers of Lepidoptera. Part I","volume":"11","author":"Bigger","year":"1960","journal-title":"Ent. Gaz."},{"key":"ref_62","first-page":"326","article-title":"The chromosomes of Erebia ligea rishirizana (Nymphalidae, Satyrinae)","volume":"20","author":"Saitoh","year":"1997","journal-title":"Nota lepid."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1163\/187631275X00091","article-title":"Chromosome numbers and notes on testicular morphology of some Lebanese Rhopalocera (Insecta Lepidoptera)","volume":"6","author":"Larsen","year":"1975","journal-title":"Entomol. Scand."},{"key":"ref_64","first-page":"332","article-title":"The butterfly chromosomes and their application in systematics and phylogeny","volume":"Volume 2","author":"Kudrna","year":"1990","journal-title":"Butterflies of Europe"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1111\/j.1095-8312.2007.00872.x","article-title":"Chromosomal evolution of South American frugivorous butterflies in the Satyroid clade (Nymphalidae: Charaxinae, Morphinae and Satyrinae)","volume":"92","author":"Brown","year":"2007","journal-title":"Biol. J. Linn. Soc."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"20","DOI":"10.3406\/bsef.1967.20914","article-title":"Formules chromosomiques de L\u00e9pidopt\u00e8res Rhopaloc\u00e8res d\u2019Afrique du Nord","volume":"72","year":"1967","journal-title":"Bull. Soc. Entomol. Fr."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1080\/21686351.1968.12278071","article-title":"Formules chromosomiques de L\u00e9pidopt\u00e8res Rhopaloc\u00e8res d\u2019Uganda et du Kenya","volume":"4","year":"1968","journal-title":"Ann. Soc. Entomol. Fr."},{"key":"ref_68","first-page":"464","article-title":"Formules chromosomiques de quelques L\u00e9pidopt\u00e8res Rhopaloc\u00e8res du S\u00e9n\u00e9gal","volume":"24","author":"Condamin","year":"1962","journal-title":"Bull. IFAN Ser. A"},{"key":"ref_69","first-page":"1089","article-title":"Formules chromosomiques de quelques L\u00e9pidopt\u00e8res Rhopaloc\u00e8res du S\u00e9n\u00e9gal et de C\u00f4te d\u2019Ivoire","volume":"27","author":"Condamin","year":"1965","journal-title":"Bull. IFAN Ser. A"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/j.cub.2018.01.061","article-title":"A comprehensive and dated phylogenomic analysis of butterflies","volume":"28","author":"Espeland","year":"2018","journal-title":"Curr. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"149","DOI":"10.3409\/fb_67-4.15","article-title":"Taxonomic rearrangement of the Erebia tyndarus species group (Lepidoptera, Nymphalidae, Satyrinae) based on an analysis of COI barcodes, morphology and geographic distribution","volume":"67","author":"Lukhtanov","year":"2019","journal-title":"Folia Biol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Lukhtanov, V.A., Dinca, V., Talavera, G., and Vila, R. (2011). Unprecedented within-species chromosome number cline in the Wood White butterfly Leptidea sinapis and its significance for karyotype evolution and speciation. BMC Evol. Biol., 11.","DOI":"10.1186\/1471-2148-11-109"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Hejn\u00ed\u010dkov\u00e1, M., Dal\u00edkov\u00e1, M., Potock\u00fd, P., Tammaru, T., Trehubenko, M., Kub\u00ed\u010dkov\u00e1, S., Marec, F., and Zrzav\u00e1, M. (2021). Degenerated, undifferentiated, rearranged, lost: High variability of sex chromosomes in Geometridae (Lepidoptera) identified by sex chromatin. Cells, 10.","DOI":"10.3390\/cells10092230"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Lucek, K. (2018). Evolutionary mechanisms of varying chromosome numbers in the radiation of Erebia butterflies. Genes, 9.","DOI":"10.3390\/genes9030166"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"20190539","DOI":"10.1098\/rstb.2019.0539","article-title":"Speciation through chromosomal fusion and fission in Lepidoptera","volume":"375","author":"Augustijnen","year":"2020","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1111\/j.1558-5646.2007.00046.x","article-title":"Karyotypic diversity and speciation in Agrodiaetus butterflies","volume":"61","author":"Kandul","year":"2007","journal-title":"Evolution"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"8199","DOI":"10.1038\/s41598-017-08525-6","article-title":"Evolutionary mechanisms of runaway chromosome number change in Agrodiaetus butterflies","volume":"7","author":"Vershinina","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1111\/j.1096-3642.2009.00627.x","article-title":"The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): A challenge for phylogenetic methods","volume":"161","author":"Nylin","year":"2011","journal-title":"Zool. J. Linn. Soc."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1862","DOI":"10.1101\/gr.276839.122","article-title":"A butterfly pan-genome reveals a large amount of structural variation underlies the evolution of chromatin accessibility","volume":"32","author":"Ruggieri","year":"2022","journal-title":"Genome Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1111\/bij.12597","article-title":"Adaptive radiations in butterflies: Evolutionary history of the genus Erebia (Nymphalidae: Satyrinae)","volume":"116","author":"Witthauer","year":"2015","journal-title":"Biol. J. Linn. Soc."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1111\/j.1601-5223.1988.tb00311.x","article-title":"Unusual sex-chromosome inheritance in six species of small ermine moths (Yponomeuta, Yponomeutidae, Lepidoptera)","volume":"108","author":"Nilsson","year":"2008","journal-title":"Hereditas"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"6931","DOI":"10.1073\/pnas.1220372110","article-title":"Neo-sex chromosomes and adaptive potential in tortricid pests","volume":"110","author":"Nguyen","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"\u0160\u00edchov\u00e1, J., Nguyen, P., Dal\u00edkov\u00e1, M., and Marec, F. (2013). Chromosomal evolution in tortricid moths: Conserved karyotypes with diverged features. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064520"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1038\/hdy.2012.84","article-title":"Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): A model of industrial melanism","volume":"110","author":"Nguyen","year":"2013","journal-title":"Heredity"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1093\/jhered\/esx063","article-title":"New insights into the evolution of the W chromosome in Lepidoptera","volume":"108","author":"Nguyen","year":"2017","journal-title":"J. Hered."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"3281","DOI":"10.1534\/g3.117.300187","article-title":"Neo-sex chromosomes in the monarch butterfly, Danaus plexippus","volume":"7","author":"Mongue","year":"2017","journal-title":"G3-Genes Genom. Genet."},{"key":"ref_87","first-page":"494852","article-title":"Chromosomal conservatism vs. chromosomal megaevolution: Enigma of karyotypic evolution in Lepidoptera","volume":"5","author":"Pazhenkova","year":"2022","journal-title":"BioRxiv"},{"key":"ref_88","unstructured":"Coyne, J.A., and Orr, H.A. (2004). Speciation, Sinauer Associates."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.tig.2008.04.007","article-title":"Sex chromosomes and speciation in Drosophila","volume":"24","author":"Presgraves","year":"2008","journal-title":"Trends Genet."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3753","DOI":"10.1111\/mec.14534","article-title":"Faster-X evolution: Theory and evidence from Drosophila","volume":"27","author":"Charlesworth","year":"2018","journal-title":"Mol. Ecol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1111\/evo.14341","article-title":"Support for faster and more adaptive Z chromosome evolution in two divergent lepidopteran lineages","volume":"76","author":"Mongue","year":"2022","journal-title":"Evolution"},{"key":"ref_92","unstructured":"King, M. (1993). Species Evolution: The Role of Chromosomal Change, Cambridge University Press."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.tree.2022.04.002","article-title":"A holocentric twist to chromosomal speciation?","volume":"37","author":"Lucek","year":"2022","journal-title":"Trends Ecol. Evol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1016\/j.tree.2010.07.008","article-title":"Chromosomal speciation revisited: Rearranging theory with pieces of evidence","volume":"25","author":"Faria","year":"2010","journal-title":"Trends Ecol. Evol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1534\/genetics.105.047985","article-title":"Chromosome inversions, local adaptation and speciation","volume":"173","author":"Kirkpatrick","year":"2006","journal-title":"Genetics"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/2\/437\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:28:45Z","timestamp":1760120925000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/2\/437"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,8]]},"references-count":95,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["genes14020437"],"URL":"https:\/\/doi.org\/10.3390\/genes14020437","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,8]]}}}