Sex chromosomes play an outsized role in adaptation and speciation, and thus deserve particular attention in evolutionary genomics. In particular, fusions between sex chromosomes and autosomes can produce neo-sex chromosomes, which offer important insights into the evolutionary dynamics of sex chromosomes. Here, we investigate the evolutionary origin of the previously reported Danaus neo-sex chromosome within the tribe Danaini. We assembled and annotated genomes of Tirumala septentrionis (subtribe Danaina), Ideopsis similis (Amaurina), Idea leuconoe (Euploeina) and Lycorea halia (Itunina) and identified their Z-linked scaffolds. We found that the Danaus neo-sex chromosome resulting from the fusion between a Z chromosome and an autosome corresponding to the Melitaea cinxia chromosome (McChr) 21 arose in a common ancestor of Danaina, Amaurina and Euploina. We also identified two additional fusions as the W chromosome further fused with the synteny block McChr31 in I. similis and independent fusion occurred between ancestral Z chromosome and McChr12 in L. halia. We further tested a possible role of sexually antagonistic selection in sex chromosome turnover by analysing the genomic distribution of sex-biased genes in I. leuconoe and L. halia. The autosomes corresponding to McChr21 and McChr31 involved in the fusions are significantly enriched in female- and male-biased genes, respectively, which could have hypothetically facilitated fixation of the neo-sex chromosomes. This suggests a role of sexual antagonism in sex chromosome turnover in Lepidoptera. The neo-Z chromosomes of both I. leuconoe and L. halia appear fully compensated in somatic tissues, but the extent of dosage compensation for the ancestral Z varies across tissues and species.

Department of Ecology and Evolutionary Biology University of Kansas Lawrence Kansas USA

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Entomology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

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Adolfsson, S. , & Ellegren, H. (2013). Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches. Molecular Biology and Evolution, 30(4), 806–810. 10.1093/molbev/mst009 PubMed DOI PMC

Ahola, V. , Lehtonen, R. , Somervuo, P. , Salmela, L. , Koskinen, P. , Rastas, P. , Välimäki, N. , Paulin, L. , Kvist, J. , Wahlberg, N. , Tanskanen, J. , Hornett, E. A. , Ferguson, L. C. , Luo, S. , Cao, Z. , de Jong, M. A. , Duplouy, A. , Smolander, O. P. , Vogel, H. , … Hanski, I. (2014). The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera. Nature Communications, 5, 4737. 10.1038/ncomms5737 PubMed DOI PMC

Anderson, N. W. , Hjelmen, C. E. , & Blackmon, H. (2020). The probability of fusions joining sex chromosomes and autosomes. Biology Letters, 16(11), 20200648. 10.1098/rsbl.2020.0648 PubMed DOI PMC

Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

Bachtrog, D. (2013). Y‐chromosome evolution: Emerging insights into processes of Y‐chromosome degeneration. Nature Reviews Genetics, 14, 113–124. 10.1038/nrg3366 PubMed DOI PMC

Bhaumik, V. , & Kunte, K. (2017). Female butterflies modulate investment in reproduction and flight in response to monsoon‐driven migrations. Oikos, 127, 285–296. 10.1111/oik.04593 DOI

Bolger, A. M. , Lohse, M. , & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Brown, K. S. , von Schoultz, B. , & Suomalainen, E. (2004). Chromosome evolution in neotropical Danainae and Ithomiinae (Lepidoptera). Hereditas, 141(3), 216–236. PubMed

Brůna, T. , Hoff, K. J. , Lomsadze, A. , Stanke, M. , & Borodovsky, M. (2021). BRAKER2: Automatic eukaryotic genome annotation with GeneMark‐EP+ and AUGUSTUS supported by a protein database. NAR Genomics and Bioinformatics, 3, lqaa108. 10.1093/nargab/lqaa108 PubMed DOI PMC

Buntrock, L. , Marec, F. , Krueger, S. , & Traut, W. (2012). Organ growth without cell division: Somatic polyploidy in a moth, Ephestia kuehniella . Genome, 55(11), 755–763. 10.1139/g2012-060 PubMed DOI

Carabajal Paladino, L. Z. , Provazníková, I. , Berger, M. , Bass, C. , Aratchige, N. S. , López, S. N. , Marec, F. , & Nguyen, P. (2019). Sex chromosome turnover in moths of the diverse superfamily Gelechioidea. Genome Biology and Evolution, 11(4), 1307–1319. 10.1093/gbe/evz075 PubMed DOI PMC

Catalan, A. , Macias‐Munoz, A. , & Briscoe, A. D. (2018). Evolution of sex‐biased gene expression and dosage compensation in the eye and brain of Heliconius butterflies. Molecular Biology and Evolution, 35(9), 2120–2134. 10.1093/molbev/msy111 PubMed DOI

Chan, P. P. , & Lowe, T. M. (2019). tRNAscan‐SE: searching for tRNA genes in genomic sequences. In Kollmar M. (Ed.), Gene prediction. Methods in molecular biology, vol. 1962 (pp. 1–14). Humana. 10.1007/978-1-4939-9173-0_1 PubMed DOI PMC

Charlesworth, D. , & Charlesworth, B. (1980). Sex differences in fitness and selection for centric fusions between sex‐chromosomes and autosomes. Genetics Research, 35(2), 205–214. 10.1017/S0016672300014051 PubMed DOI

Chazot, N. , Willmott, K. R. , Lamas, G. , Freitas, A. V. L. , Piron‐Prunier, F. , Arias, C. F. , Mallet, J. , de‐Silva, D. L. , & Elias, M. (2019). Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation. Global Ecology and Biogeography, 28(8), 1118–1132. 10.1111/geb.12919 DOI

Cheng, C. D. , & Kirkpatrick, M. (2016). Sex‐specific selection and sex‐biased gene expression in humans and flies. PLoS Genetics, 12(9), e1006170. 10.1371/journal.pgen.1006170 PubMed DOI PMC

Dagilis, A. J. , Sardell, J. M. , Josephson, M. P. , Su, Y. H. , Kirkpatrick, M. , & Peichel, C. L. (2022). Searching for signatures of sexually antagonistic selection on stickleback sex chromosomes. Philosophical Transactions of the Royal Society, B: Biological Sciences, 377(1856), 20210205. 10.1098/rstb.2021.0205 PubMed DOI PMC

Dapper, A. L. , & Wade, M. J. (2020). Relaxed selection and the rapid evolution of reproductive genes. Trends in Genetics, 36(9), 640–649. 10.1016/j.tig.2020.06.014 PubMed DOI

De Coster, W. , D'Hert, S. , Schultz, D. T. , Cruts, M. , & Van Broeckhoven, C. (2018). NanoPack: Visualizing and processing long‐read sequencing data. Bioinformatics, 34(15), 2666–2669. 10.1093/bioinformatics/bty149 PubMed DOI PMC

Delhomme, N. , Padioleau, I. , Furlong, E. E. , & Steinmetz, L. M. (2012). easyRNASeq: A bioconductor package for processing RNA‐Seq data. Bioinformatics, 28(19), 2532–2533. 10.1093/bioinformatics/bts477 PubMed DOI PMC

Dobin, A. , & Gingeras, T. R. (2015). Mapping RNA‐seq reads with STAR. Current Protocols in Bioinformatics, 51, 11141‐19. 10.1002/0471250953.bi1114s51 PubMed DOI PMC

Ellegren, H. (2011). Sex‐chromosome evolution: Recent progress and the influence of male and female heterogamety. Nature Reviews Genetics, 12(3), 157–166. 10.1038/nrg2948 PubMed DOI

Filatov, D. A. (2018). The two "rules of speciation" in species with young sex chromosomes. Molecular Ecology, 27(19), 3799–3810. 10.1111/mec.14721 PubMed DOI

Flynn, J. M. , Hubley, R. , Goubert, C. , Rosen, J. , Clark, A. G. , Feschotte, C. , & Smit, A. F. (2020). RepeatModeler2 for automated genomic discovery of transposable element families. Proceedings of National Academy of Sciences USA, 117(17), 9451–9457. 10.1073/pnas.1921046117 PubMed DOI PMC

Fraïsse, C. , Picard, M. A. L. , & Vicoso, B. (2017). The deep conservation of the Lepidoptera Z chromosome suggests a non‐canonical origin of the W. Nature Communications, 8(1), 1486. 10.1038/s41467-017-01663-5 PubMed DOI PMC

Furman, B. L. S. , Metzger, D. C. H. , Darolti, I. , Wright, A. E. , Sandkam, B. A. , Almeida, P. , Shu, J. J. , & Mank, J. E. (2020). Sex chromosome evolution: So many exceptions to the rules. Genome Biology and Evolution, 12(6), 750–763. 10.1093/gbe/evaa081 PubMed DOI PMC

Grath, S. , & Parsch, J. (2016). Sex‐biased gene expression. Annual Review of Genetics, 50, 29–44. PubMed

Graves, J. A. M. (2016). Did sex chromosome turnover promote divergence of the major mammal groups?: De novo sex chromosomes and drastic rearrangements may have posed reproductive barriers between monotremes, marsupials and placental mammals. BioEssays, 38(8), 734–743. 10.1002/bies.201600019 PubMed DOI PMC

Graves, J. A. M. , & Peichel, C. L. (2010). Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biology, 11(4), 205. 10.1186/gb-2010-11-4-205 PubMed DOI PMC

Gu, L. , Reilly, P. F. , Lewis, J. J. , Reed, R. D. , Andolfatto, P. , & Walters, J. R. (2019). Dichotomy of dosage compensation along the neo Z chromosome of the monarch butterfly. Current Biology, 29(23), 4071–4077. 10.1016/j.cub.2019.09.056 PubMed DOI PMC

Gu, L. Q. , & Walters, J. R. (2017). Evolution of sex chromosome dosage compensation in animals: A beautiful theory, undermined by facts and bedeviled by details. Genome Biology and Evolution, 9(9), 2461–2476. 10.1093/gbe/evx154 PubMed DOI PMC

Gu, L. Q. , Walters, J. R. , & Knipple, D. C. (2017). Conserved patterns of sex chromosome dosage compensation in the Lepidoptera (WZ/ZZ): Insights from a moth neo‐Z chromosome. Genome Biology and Evolution, 9(3), 802–816. 10.1093/gbe/evx039 PubMed DOI PMC

Guan, D. , McCarthy, S. A. , Wood, J. , Howe, K. , Wang, Y. , & Durbin, R. (2020). Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics, 36(9), 2896–2898. 10.1093/bioinformatics/btaa025 PubMed DOI PMC

Herbert, P. N. D. , Penton, E. H. , Burns, J. M. , Janzen, D. H. , & Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proceedings of the National Academy of Sciences, 101(41), 14812–14817. 10.1073/pnas.04061661 PubMed DOI PMC

Hill, J. , Rastas, P. , Hornett, E. A. , Neethiraj, R. , Clark, N. , Morehouse, N. , de la Paz Celorio‐Mancera, M. , Cols, J. C. , Dircksen, H. , Meslin, C. , Keehnen, N. , Pruisscher, P. , Sikkink, K. , Vives, M. , Vogel, H. , Wiklund, C. , Woronik, A. , Boggs, C. L. , Nylin, S. , & Wheat, C. W. (2019). Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Science Advances, 5(6), eaau3648. 10.1126/sciadv.aau3648 PubMed DOI PMC

Holley, G. , Beyter, D. , Ingimundardottir, H. , Møller, P. L. , Kristmundsdottir, S. , Eggertsson, H. P. , & Halldorsson, B. V. (2021). Ratatosk: Hybrid error correction of long reads enables accurate variant calling and assembly. Genome Biology, 22(1), 28. 10.1186/s13059-020-02244-4 PubMed DOI PMC

Hu, J. , Fan, J. , Sun, Z. , & Liu, S. (2020). NextPolish: A fast and efficient genome polishing tool for long‐read assembly. Bioinformatics, 36(7), 2253–2255. 10.1093/bioinformatics/btz891 PubMed DOI

Humann, J. L. , Lee, T. , Ficklin, S. , & Main, D. (2019). Structural and functional annotation of eukaryotic genomes with GenSAS. In Kollmar M. (Ed.), Gene Prediction. Methods in Molecular Biology, vol. 1962. Humana. 10.1007/978-1-4939-9173-0_3 PubMed DOI

Huylmans, A. K. , Macon, A. , & Vicoso, B. (2017). Global dosage compensation is ubiquitous in Lepidoptera, but counteracted by the masculinization of the Z chromosome. Molecular Biology and Evolution, 34(10), 2637–2649. 10.1093/molbev/msx190 PubMed DOI PMC

Innocenti, P. , & Morrow, E. H. (2010). The sexually antagonistic genes of Drosophila melanogaster . PLoS Biology, 8(3), e1000335. 10.1371/journal.pbio.1000335 PubMed DOI PMC

Kirkpatrick, M. , & Guerrero, R. F. (2014). Signatures of sex‐antagonistic selection on recombining sex chromosomes. Genetics, 197(2), 531. 10.1534/genetics.113.156026 PubMed DOI PMC

Kitano, J. , & Peichel, C. L. (2012). Turnover of sex chromosomes and speciation in fishes. Environmental Biology of Fishes, 94(3), 549–558. 10.1007/s10641-011-9853-8 PubMed DOI PMC

Kitano, J. , Ross, J. A. , Mori, S. , Kume, M. , Jones, F. C. , Chan, Y. F. , Absher, D. M. , Grimwood, J. , Schmutz, J. , Myers, R. M. , Kingsley, D. M. , & Peichel, C. L. (2009). A role for a neo‐sex chromosome in stickleback speciation. Nature, 461(7267), 1079–1083. 10.1038/nature08441 PubMed DOI PMC

Kiuchi, T. , Koga, H. , Kawamoto, M. , Shoji, K. , Sakai, H. , Arai, Y. , Ishihara, G. , Kawaoka, S. , Sugano, S. , Shimada, T. , Suzuki, Y. , Suzuki, M. G. , & Katsuma, S. (2014). A single female‐specific piRNA is the primary determiner of sex in the silkworm. Nature, 509, 633–636. 10.1038/nature13315 PubMed DOI

Kolmogorov, M. , Yuan, J. , Lin, Y. , & Pevzner, P. A. (2019). Assembly of long, error‐prone reads using repeat graphs. Nature Biotechnology, 37(5), 540–546. 10.1038/s41587-019-0072-8 PubMed DOI

Kopylova, E. , Noé, L. , & Touzet, H. (2012). SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics, 28(24), 3211–3217. 10.1093/bioinformatics/bts611 PubMed DOI

Kurtz, S. , Phillippy, A. , Delcher, A. L. , Smoot, M. , Shumway, M. , Antonescu, C. , & Salzberg, S. L. (2004). Versatile and open software for comparing large genomes. Genome Biology, 5(2), R12. 10.1186/gb-2004-5-2-r12 PubMed DOI PMC

Laetsch, D. R. , & Blaxter, M. L. (2017). BlobTools: Interrogation of genome assemblies. F1000Research, 6, 1287. 10.12688/f1000research.12232.1 DOI

Lagesen, K. , Hallin, P. , Rødland, E. A. , Stærfeldt, H.‐H. , Rognes, T. , & Ussery, D. W. (2007). RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Research, 35(9), 3100–3108. 10.1093/nar/gkm160 PubMed DOI PMC

Langmead, B. , & Salzberg, S. L. (2012). Fast gapped‐read alignment with bowtie 2. Nature Methods, 9(4), 357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Lasne, C. , Sgro, C. M. , & Connallon, T. (2017). The relative contributions of the X chromosome and autosomes to local adaptation. Genetics, 205(3), 1285–1304. 10.1534/genetics.116.194670 PubMed DOI PMC

Li, H. , Handsaker, B. , Wysoker, A. , Fennell, T. , Ruan, J. , Homer, N. , Marth, G. , Abecasis, G. , & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC

Liao, Y. , Smyth, G. K. , & Shi, W. (2014). featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30(7), 923–930. 10.1093/bioinformatics/btt656 PubMed DOI

Lichilin, N. , El Taher, A. , & Bohne, A. (2021). Sex‐biased gene expression and recent sex chromosome turnover. Philosophical Transactions of the Royal Society, B: Biological Sciences, 376(1833), 20200107. 10.1098/rstb.2020.0107 PubMed DOI PMC

Lomsadze, A. , Burns, P. D. , & Borodovsky, M. (2014). Integration of mapped RNA‐Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Research, 42(15), e119. 10.1093/nar/gku557 PubMed DOI PMC

Love, M. I. , Huber, W. , & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biology, 15(12), 550. 10.1186/s13059-014-0550-8 PubMed DOI PMC

Lucek, K. , Giménez, M. D. , Joron, M. , Rafajlović, M. , Searle, J. B. , Walden, N. , Westram, A. M. , & Faria, R. (2023). The impact of chromosomal rearrangements in speciation: From micro‐ to macroevolution. Cold Spring Harbor Perspectives in Biology, 15, a041447. 10.1101/cshperspect.a041447 PubMed DOI PMC

Lund‐Hansen, K. K. , Olito, C. , Morrow, E. H. , & Abbott, J. K. (2021). Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster . Proceedings of the National Academy of Sciences of the United States of America, 118(8), e2003359118. 10.1073/pnas.2003359118 PubMed DOI PMC

Maeki, K. , & Ae, S. A. (1969). Studies of the chromosomes of Formosan Rhopalocera 4. Danaidae and Satyridae. Kontyu, 37(1), 99–109.

Mank, J. E. (2017). The transcriptional architecture of phenotypic dimorphism. Nature Ecology & Evolution, 1(1). 10.1038/s41559-016-0006 PubMed DOI

Mank, J. E. , & Ellegren, H. (2009). Sex‐linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Evolution, 63(6), 1464–1472. 10.1111/j.1558-5646.2009.00618.x PubMed DOI

Mank, J. E. , Hosken, D. J. , & Wedell, N. (2014). Conflict on the sex chromosomes: Cause, effect, and complexity. Cold Spring Harbor Perspectives in Biology, 6(12), a017715. 10.1101/cshperspect.a017715 PubMed DOI PMC

Manni, M. , Berkeley, M. R. , Seppey, M. , Simão, F. A. , & Zdobnov, E. M. (2021). BUSCO update: Novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Molecular Biology and Evolution, 38(10), 4647–4654. 10.1093/molbev/msab199 PubMed DOI PMC

Marçais, G. , & Kingsford, C. (2011). A fast, lock‐free approach for efficient parallel counting of occurrences of k‐mers. Bioinformatics, 27(6), 764–770. 10.1093/bioinformatics/btr011 PubMed DOI PMC

Marec, F. (1996). Synaptonemal complexes in insects. International Journal of Insect Morphology and Embryology, 25(3), 205–233. 10.1016/0020-7322(96)00009-8 DOI

Martin, M. (2011). Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet.Journal, 17(1), 10–12.

Martin, S. H. , Singh, K. S. , Gordon, I. J. , Omufwoko, K. S. , Collins, S. , Warren, I. A. , Munby, H. , Brattström, O. , Traut, W. , Martins, D. J. , Smith, D. A. S. , Jiggins, C. D. , Bass, C. , & French‐Constant, R. H. (2020). Whole‐chromosome hitchhiking driven by a male‐killing endosymbiont. PLoS Biology, 18(2), e3000610. 10.1371/journal.pbio.3000610 PubMed DOI PMC

Matsumoto, T. , Yoshida, K. , & Kitano, J. (2016). Gene flow and sex chromosome evolution. Genes & Genetic Systems, 91(6), 357.

McAllister, B. F. , Sheeley, S. L. , Mena, P. A. , Evans, A. L. , & Schlotterer, C. (2008). Clinal distribution of a chromosomal rearrangement: A precursor to chromosomal speciation? Evolution, 62(8), 1852–1865. 10.1111/j.1558-5646.2008.00435.x PubMed DOI

Mediouni, J. , Fukova, I. , Frydrychova, R. , Dhouibi, M. H. , & Marec, F. (2004). Karyotype, sex chromatin and sex chromosome differentiation in the carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). Caryologia, 57(2), 184–194.

Mongue, A. J. , Hansen, M. E. , & Walters, J. R. (2022). Support for faster and more adaptive Z chromosome evolution in two divergent lepidopteran lineages. Evolution, 76(2), 332–345. 10.1111/evo.14341 PubMed DOI PMC

Mongue, A. J. , Nguyen, P. , Voleníková, A. , & Walters, J. R. (2017). Neo‐sex chromosomes in the monarch butterfly, Danaus plexippus . G3: Genes, Genomes, Genetics, 7(10), 3281–3294. 10.1534/g3.117.300187 PubMed DOI PMC

Mongue, A. J. , & Walters, J. R. (2018). The Z chromosome is enriched for sperm proteins in two divergent species of Lepidoptera. Genome, 61(4), 248–253. 10.1139/gen-2017-0068 PubMed DOI

Mora, P. , Hospodarska, M. , Volenikova, A. , Koutecky, P. , Stundlova, J. , Dalikova, M. , Walters, J. R. , & Nguyen, P. (2023). Sex chromosome evolution in the tribe Danaini. Dryad, Dataset . 10.5061/dryad.hmgqnk9p2 PubMed DOI PMC

Nguyen, P. , & Carabajal Paladino, L. (2016). On the neo‐sex chromosomes of Lepidoptera. In Pontarotti P. (Ed.), Evolutionary biology: Convergent evolution, evolution of complex traits, concepts and methods (pp. 171–185). Springer.

Nguyen, P. , Sýkorová, M. , Šíchová, J. , Kůta, V. , Dalíková, M. , Čapková Frydrychová, R. , Neven, L. G. , Sahara, K. , & Marec, F. (2013). Neo‐sex chromosomes and adaptive potential in tortricid pests. Proceedings of the National Academy of Sciences, 110(17), 6931–6936. 10.1073/pnas.1220372110 PubMed DOI PMC

Novák, P. , Ávila Robledillo, L. , Koblížková, A. , Vrbová, I. , Neumann, P. , & Macas, J. (2017). TAREAN: A computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Research, 45(12), e111. 10.1093/nar/gkx257 PubMed DOI PMC

O'Meally, D. , Ezaz, T. , Georges, A. , Sarre, S. D. , & Graves, J. A. M. (2012). Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Research, 20(1), 7–19. 10.1007/s10577-011-9266-8 PubMed DOI

Oshlack, A. , Robinson, M. D. , & Young, M. D. (2010). From RNA‐seq reads to differential expression results. Genome Biology, 11(12), 220. 10.1186/gb-2010-11-12-220 PubMed DOI PMC

Palmer, D. H. , Rogers, T. F. , Dean, R. , & Wright, A. E. (2019). How to identify sex chromosomes and their turnover. Molecular Ecology, 28(21), 4709–4724. 10.1111/mec.15245 PubMed DOI PMC

Pan, Q. W. , Kay, T. , Depince, A. , Adolfi, M. , Schartl, M. , Guiguen, Y. , & Herpin, A. (2021). Evolution of master sex determiners: TGF‐beta signalling pathways at regulatory crossroads. Philosophical Transactions of the Royal Society, B: Biological Sciences, 376(1832), 20200091. 10.1098/rstb.2020.0091 PubMed DOI PMC

Parsch, J. , & Ellegren, H. (2013). The evolutionary causes and consequences of sex‐biased gene expression. Nature Reviews Genetics, 14(2), 83–87. 10.1038/nrg3376 PubMed DOI

Payseur, B. A. , Presgraves, D. C. , & Filatov, D. A. (2018). Introduction: Sex chromosomes and speciation. Molecular Ecology, 27(19), 3745–3748. 10.1111/mec.14828 PubMed DOI PMC

Pedersen, B. S. , Collins, R. L. , Talkowski, M. E. , & Quinlan, A. R. (2017). Indexcov: Fast coverage quality control for whole‐genome sequencing. GigaScience, 6(11), 1–6. 10.1093/gigascience/gix090 PubMed DOI PMC

Pennell, M. W. , Kirkpatrick, M. , Otto, S. P. , Vamosi, J. C. , Peichel, C. L. , Valenzuela, N. , & Kitano, J. (2015). Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genetics, 11(5), e1005237. 10.1371/journal.pgen.1005237 PubMed DOI PMC

Perrin, N. (2021). Sex‐chromosome evolution in frogs: What role for sex‐antagonistic genes? Philosophical Transactions of the Royal Society, B: Biological Sciences, 376(1832), 20200094. 10.1098/rstb.2020.0094 PubMed DOI PMC

Pohlert, T. (2022). PMCMRplus: Calculate pairwise multiple comparisons of mean rank sums extended.

Pokorna, M. , Altmanova, M. , & Kratochvil, L. (2014). Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Research, 22(1), 35–44. 10.1007/s10577-014-9403-2 PubMed DOI

Provaznikova, I. , Dalikova, M. , Volenikova, A. , Roessingh, P. , Sahara, K. , Provaznik, J. , Marec, F. , & Nguyen, P. (2023). Multiple sex chromosomes of Yponomeuta ermine moths suggest a role of sexual antagonism in sex chromosome turnover in Lepidoptera. bioRxiv . 10.1101/2023.06.06.543653 DOI

Quinlan, A. R. , & Hall, I. M. (2010). BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics, 26(6), 841–842. 10.1093/bioinformatics/btq033 PubMed DOI PMC

Ranz, J. M. , González, P. M. , Clifton, B. D. , Nazario‐Yepiz, N. O. , Hernández‐Cervantes, P. L. , Palma‐Martínez, M. J. , Valdivia, D. I. , Jiménez‐Kaufman, A. , Lu, M. M. , Markow, T. A. , & Abreu‐Goodger, C. (2021). A de novo transcriptional atlas in Danaus plexippus reveals variability in dosage compensation across tissues. Communications Biology, 4, 791. 10.1038/s42003-021-02335-3 PubMed DOI PMC

Rice, W. R. (1984). Sex‐chromosomes and the evolution of sexual dimorphism. Evolution, 38(4), 735–742. 10.2307/2408385 PubMed DOI

Rice, W. R. (1987). The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution, 41(4), 911–914. 10.1111/j.1558-5646.1987.tb05864.x PubMed DOI

Robinson, M. D. , & Oshlack, A. (2010). A scaling normalization method for differential expression analysis of RNA‐seq data. Genome Biology, 11(3), R25. 10.1186/gb-2010-11-3-r25 PubMed DOI PMC

Ross, J. A. , Urton, J. R. , Boland, J. , Shapiro, M. D. , & Peichel, C. L. (2009). Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genetics, 5(2), e1000391. 10.1371/journal.pgen.1000391 PubMed DOI PMC

Sahara, K. , Marec, F. , & Traut, W. (1999). TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Research, 7(6), 449–460. 10.1023/a:1009297729547 PubMed DOI

Schurch, N. J. , Schofield, P. , Gierliński, M. , Cole, C. , Sherstnev, A. , Singh, V. , Wrobel, N. , Gharbi, K. , Simpson, G. G. , Owen‐Hughes, T. , Blaxter, M. , & Barton, G. J. (2016). How many biological replicates are needed in an RNA‐seq experiment and which differential expression tool should you use? RNA, 22(6), 839–851. 10.1261/rna.053959.115 PubMed DOI PMC

Šíchová, J. , Nguyen, P. , Dalíková, M. , & Marec, F. (2013). Chromosomal evolution in tortricid moths: Conserved karyotypes with diverged features. PLoS One, 8(5), e64520. 10.1371/journal.pone.0064520 PubMed DOI PMC

Šíchová, J. , Voleníková, A. , Dincă, V. , Nguyen, P. , Vila, R. , Sahara, K. , & Marec, F. (2015). Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evolutionary Biology, 15, 89. 10.1186/s12862-015-0375-4 PubMed DOI PMC

Sigeman, H. , Ponnikas, S. , Chauhan, P. , Dierickx, E. , Brooke, M. D. , & Hanssonl, B. (2019). Repeated sex chromosome evolution in vertebrates supported by expanded avian sex chromosomes. Proceedings of the Royal Society B: Biological Sciences, 286(1916), 20192051. 10.1098/rspb.2019.2051 PubMed DOI PMC

Singh, K. S. , De‐Kayne, R. , Omufwoko, K. S. , Martins, D. J. , Bass, C. , French‐Constant, R. , & Martin, S. H. (2022). Genome assembly of Danaus chrysippus and comparison with the monarch Danaus plexippus . G3: Genes, Genomes, Genetics, 12, jkab449. 10.1093/g3journal/jkab449 PubMed DOI PMC

Smit, A. F. A. , Hubley, R. , & Green, P. (2013. ‐2015). RepeatMasker Open‐4.0. http://www.repeatmasker.org

Smith, D. A. S. , Gordon, I. J. , Traut, W. , Herren, J. , Collins, S. , Martins, D. J. , Saitoti, K. , Ireri, P. , & French‐Constant, R. (2016). A neo‐W chromosome in a tropical butterfly links colour pattern, male‐killing, and speciation. Proceedings of the Royal Society B: Biological Sciences, 283(1835), 20160821. 10.1098/rspb.2016.0821 PubMed DOI PMC

Smolander, O.‐P. , Blande, D. , Ahola, V. , Rastas, P. , Tanskanen, J. , Kammonen, J. I. , Oostra, V. , Pellegrini, L. , Ikonen, S. , Dallas, T. , DiLeo, M. F. , Duplouy, A. , Duru, I. C. , Halimaa, P. , Kahilainen, A. , Kuwar, S. S. , Kärenlampi, S. O. , Lafuente, E. , Luo, S. , … Saastamoinen, M. (2022). Improved chromosome‐level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) integrating Pacific biosciences long reads and a high‐density linkage map. GigaScience, 11, giab097. 10.1093/gigascience/giab097 PubMed DOI PMC

Stanke, M. , & Morgenstern, B. (2005). AUGUSTUS: A web server for gene prediction in eukaryotes that allows user‐defined constraints. Nucleic Acids Research, 33, W465–W467. 10.1093/nar/gki458 PubMed DOI PMC

Steward, R. A. , Okamura, Y. , Boggs, C. L. , Vogel, H. , & Wheat, C. W. (2021). The genome of the margined white butterfly (Pieris macdunnoughii): Sex chromosome insights and the power of polishing with PoolSeq data. Genome Biology and Evolution, 13(4), evab053. 10.1093/gbe/evab053 PubMed DOI PMC

Suetsugu, Y. , Futahashi, R. , Kanamori, H. , Kadono‐Okuda, K. , Sasanuma, S.‐I. , Narukawa, J. , Ajimura, M. , Jouraku, A. , Namiki, N. , Shimomura, M. , Sezutsu, H. , Osanai‐Futahashi, M. , Suzuki, M. G. , Daimon, T. , Shinoda, T. , Taniai, K. , Asaoka, K. , Niwa, R. , Kawaoka, S. , … Mita, K. (2013). Large scale full‐length cDNA sequencing reveals a unique genomic landscape in a lepidopteran model insect, Bombyx mori. G3: Genes, Genomes, Genetics, 3(9), 1481–1492. 10.1534/g3.113.006239 PubMed DOI PMC

Toups, M. A. , & Vicoso, B. (2023). The X chromosome of insects likely predates the origin of class Insecta. Evolution, 77(11), 2504–2511. 10.1093/evolut/qpad169 PubMed DOI

Traut, W. , Schubert, V. , Dalikova, M. , Marec, F. , & Sahara, K. (2019). Activity and inactivity of moth sex chromosomes in somatic and meiotic cells. Chromosoma, 128(4), 533–545. 10.1007/s00412-019-00722-8 PubMed DOI

Veltsos, P. , Rodrigues, N. , Studer, T. , Ma, W. J. , Sermier, R. , Leuenberger, J. , & Perrin, N. (2020). No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs. Journal of Evolutionary Biology, 33(4), 401–409. 10.1111/jeb.13573 PubMed DOI

Vicoso, B. , & Charlesworth, B. (2006). Evolution on the X chromosome: Unusual patterns and processes. Nature Reviews Genetics, 7(8), 645–653. 10.1038/nrg1914 PubMed DOI

Vurture, G. W. , Sedlazeck, F. J. , Nattestad, M. , Underwood, C. J. , Fang, H. , Gurtowski, J. , & Schatz, M. C. (2017). GenomeScope: Fast reference‐free genome profiling from short reads. Bioinformatics, 33(14), 2202–2204. 10.1093/bioinformatics/btx153 PubMed DOI PMC

Walters, J. R. , & Hardcastle, T. J. (2011). Getting a full dose? Reconsidering sex chromosome dosage compensation in the silkworm, Bombyx mori . Genome Biology and Evolution, 3, 491–504. 10.1093/gbe/evr036 PubMed DOI PMC

Walters, J. R. , Hardcastle, T. J. , & Jiggins, C. D. (2015). Sex chromosome dosage compensation in Heliconius butterflies: Global yet still incomplete? Genome Biology and Evolution, 7(9), 2545–2559. 10.1093/gbe/evv156 PubMed DOI PMC

Wright, A. E. , Dean, R. , Zimmer, F. , & Mank, J. E. (2016). How to make a sex chromosome. Nature Communications, 7, 12087. 10.1038/ncomms12087 PubMed DOI PMC

Wright, C. J. , Stevens, L. , Mackintosh, A. , Lawniczak, M. , & Blaxter, M. (2023). Chromosome Evolution in Lepidoptera. ssiv . 10.1101/2023.05.12.540473 PubMed DOI PMC

Yoshido, A. , Šíchová, J. , Pospíšilová, K. , Nguyen, P. , Voleníková, A. , Šafář, J. , Provazník, J. , Vila, R. , & Marec, F. (2020). Evolution of multiple sex‐chromosomes associated with dynamic genome reshuffling in Leptidea wood‐white butterflies. Heredity, 125(3), 138–154. 10.1038/s41437-020-0325-9 PubMed DOI PMC

Sex-biased gene content is associated with sex chromosome turnover in Danaini butterflies

Satellite DNAs and the evolution of the multiple X1X2Y sex chromosomes in the wolf fish Hoplias malabaricus (Teleostei; Characiformes)