Sex Chromosomes of the Iconic Moth Abraxas grossulariata (Lepidoptera, Geometridae) and Its Congener A. sylvata

. 2018 May 31 ; 9 (6) : . [epub] 20180531

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29857494

The magpie moth, Abraxas grossulariata, is an iconic species in which female heterogamety was discovered at the beginning of the 20th century. However, the sex chromosomes of this species have not yet been cytologically identified. We describe the sex chromosomes of A. grossulariata and its congener, A. sylvata. Although these species split only around 9.5 million years ago, and both species have the expected WZ/ZZ chromosomal system of sex determination and their sex chromosomes share the major ribosomal DNA (rDNA) representing the nucleolar organizer region (NOR), we found major differences between their karyotypes, including between their sex chromosomes. The species differ in chromosome number, which is 2n = 56 in A. grossularita and 2n = 58 in A. sylvata. In addition, A. grossularita autosomes exhibit massive autosomal blocks of heterochromatin, which is a very rare phenomenon in Lepidoptera, whereas the autosomes of A. sylvata are completely devoid of distinct heterochromatin. Their W chromosomes differ greatly. Although they are largely composed of female-specific DNA sequences, as shown by comparative genomic hybridization, cross-species W-chromosome painting revealed considerable sequence differences between them. The results suggest a relatively rapid molecular divergence of Abraxas W chromosomes by the independent spreading of female-specific repetitive sequences.

Zobrazit více v PubMed

Stevens N.M. Carnegie Institution of Washington, Publication No. 36. Henry E. Wilkens Printing Co.; Washington, DC, USA: 1905. Studies in spermatogenesis with especial reference to the “accessory chromosome”.33p

Morgan T.H., Sturtevant A.H., Muller H.J., Bridges C.B. The Mechanism of Mendelian Heredity. Henry Holt and Company; New York, NY, USA: 1915. 262p

Doncaster L., Raynor G.H. On breeding experiments with Lepidoptera. Proc. Zool. Soc. Lond. 1906;1:125–133. doi: 10.1111/j.1469-7998.1906.tb08425.x. DOI

Doncaster L. The chromosomes in the oogenesis and spermatogenesis of Pieris brassicae, and in the oogenesis of Abraxas grossulariata. J. Genet. 1912;2:189–200. doi: 10.1007/BF02981539. DOI

Seiler J. Geschlechtschromosomen bei Lepidopteren. Zool. Anz. 1913;41:246–251.

Traut W., Sahara K., Marec F. Sex chromosomes and sex determination in Lepidoptera. Sex. Dev. 2007;1:332–346. doi: 10.1159/000111765. PubMed DOI

Marec F., Sahara K., Traut W. Rise and fall of the W chromosome in Lepidoptera. In: Goldsmith M.R., Marec F., editors. Molecular Biology and Genetics of the Lepidoptera. CRC Press; Boca Raton, FL, USA: 2010. pp. 49–63.

Sahara K., Yoshido A., Traut W. Sex chromosome evolution in moths and butterflies. Chromosome Res. 2012;20:83–94. doi: 10.1007/s10577-011-9262-z. PubMed DOI

Dopman E.B., Perez L., Bogdanowicz S.M., Harrison R.G. Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proc. Natl. Acad. Sci. USA. 2005;102:14706–14711. doi: 10.1073/pnas.0502054102. PubMed DOI PMC

Putnam A.S., Scriber J.M., Andolfatto P. Discordant divergence times among Z-chromosome regions between two ecologically distinct swallowtail butterfly species. Evolution. 2007;61:912–927. doi: 10.1111/j.1558-5646.2007.00076.x. PubMed DOI

Nguyen P., Sýkorová M., Šíchová J., Kůta V., Dalíková M., Čapková Frydrychová R., Neven L.G., Sahara K., Marec F. Neo-sex chromosomes and adaptive potential in tortricid pests. Proc. Natl. Acad. Sci. USA. 2013;110:6931–6936. doi: 10.1073/pnas.1220372110. PubMed DOI PMC

Kiuchi T., Koga H., Kawamoto M., Shoji K., Sakai H., Arai Y., Ishihara G., Kawaoka S., Sugano S., Shimada T., et al. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature. 2014;509:633–636. doi: 10.1038/nature13315. PubMed DOI

Kost S., Heckel D.G., Yoshido A., Marec F., Groot A.T. A Z-linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda. Evolution. 2016;70:1418–1427. doi: 10.1111/evo.12940. PubMed DOI

Graves J.A.M. Evolution of vertebrate sex chromosomes and dosage compensation. Nat. Rev. Genet. 2016;17:33–46. doi: 10.1038/nrg.2015.2. PubMed DOI

Schartl M., Schmid M., Nanda I. Dynamics of vertebrate sex chromosome evolution: From equal size to giants and dwarfs. Chromosoma. 2016;125:553–571. doi: 10.1007/s00412-015-0569-y. PubMed DOI

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

Bush G.L. Female heterogamety in the family Tephritidae (Acalyptratae, Diptera) Am. Nat. 1966;100:119–126. doi: 10.1086/282405. DOI

Kaiser V.B., Bachtrog D. Evolution of sex chromosomes in insects. Annu. Rev. Genet. 2010;44:91–112. doi: 10.1146/annurev-genet-102209-163600. PubMed DOI PMC

Rigaud T., Juchault P., Mocquard J.P. The evolution of sex determination in isopod crustaceans. BioEssays. 1997;19:409–416. doi: 10.1002/bies.950190508. DOI

Špakulová M., Casanova J.C. Current knowledge on B chromosomes in natural populations of helminth parasites: A review. Cytogenet. Genome Res. 2004;106:222–229. doi: 10.1159/000079291. PubMed DOI

Kongim B., Sutcharit C., Tongkerd P., Tan S.H.A., Quynh N.X., Naggs F., Panha S. Karyotype variations in the genus Pollicaria (Caenogastropoda: Pupinidae) Zool. Stud. 2010;49:125–131.

Parnes S., Khalaila I., Hulata G., Sagi A. Sex determination in crayfish: Are intersex Cherax quadricarinatus (Decapoda, Parastacidae) genetically females? Genet. Res. 2003;82:107–116. doi: 10.1017/S0016672303006372. PubMed DOI

Jiang X.H., Qiu G.F. Female-only sex-linked amplified fragment length polymorphism markers support ZW/ZZ sex determination in the giant freshwater prawn Macrobrachium rosenbergii. Anim. Genet. 2013;44:782–785. doi: 10.1111/age.12067. PubMed DOI

Kumar S., Kumari R., Sharma V. Genetics of dioecy and causal sex chromosomes in plants. J. Genet. 2014;93:241–277. doi: 10.1007/s12041-014-0326-7. PubMed DOI

Van Nieukerken E.J., Kaila L., Kitching I.J., Kristensen N.P., Lees D.C., Minet J., Mitter C., Mutanen M., Regier J.C., Simonsen T.J., et al. Order Lepidoptera Linnaeus, 1758. In: Zhang Z.Q., editor. Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness. Magnolia Press; Auckland, New Zealand: 2011.

Šíchová J., Voleníková A., Dincă V., Nguyen P., Vila R., Sahara K., Marec F. 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

Šíchová J., Ohno M., Dincă V., Watanabe M., Sahara K., Marec F. Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis. Biol. J. Linn. Soc. 2016;118:457–471. doi: 10.1111/bij.12756. 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

Nguyen P., Carabajal Paladino L. On the neo-sex chromosomes of Lepidoptera. In: Pontarotti P., editor. Evolutionary Biology. Springer International Publishing; Cham, Switzerland: 2016. pp. 171–185.

Traut W., Sahara K., Otto T.D., Marec F. Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma. 1999;108:173–180. doi: 10.1007/s004120050366. PubMed DOI

Vítková M., Fuková I., Kubíčková S., Marec F. Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera) Chromosome Res. 2007;15:917–930. doi: 10.1007/s10577-007-1173-7. PubMed DOI

Van’t Hof A.E., Nguyen P., Dalíková M., Edmonds N., Marec F., Saccheri I.J. Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): A model of industrial melanism. Heredity. 2013;110:283–295. doi: 10.1038/hdy.2012.84. PubMed DOI PMC

Dalíková M., Zrzavá M., Hladová I., Nguyen P., Šonský I., Flegrová M., Kubíčková S., Voleníková A., Kawahara A.Y., Peters R.S., 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

Fraïsse C., Picard M.A.L., 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

Asser-Kaiser S., Fritsch E., Undorf-Spahn K., Kienzle J., Eberle K.E., Gund N.A., Reineke A., Zebitz C.P.W., Heckel D.G., Huber J., 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

Mank J.E., Nam K., Ellegren H. Faster-Z evolution is predominantly due to genetic drift. Mol. Biol. Evol. 2010;27:661–670. doi: 10.1093/molbev/msp282. PubMed DOI

Sackton T.B., Corbett-Detig R.B., Nagaraju J., Vaishna L., Arunkumar K.P., Hartl D.L. Positive selection drives faster-Z evolution in silkmoths. Evolution. 2014;68:2331–2342. doi: 10.1111/evo.12449. PubMed DOI PMC

Abe H., Mita K., Yasukochi Y., Oshiki T., Shimada T. Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet. Genome Res. 2005;110:144–151. doi: 10.1159/000084946. PubMed DOI

Fuková I., Traut W., Vítková M., Nguyen P., Kubíčková S., Marec F. Probing the W chromosome of the codling moth, Cydia pomonella, with sequences from microdissected sex chromatin. Chromosoma. 2007;116:135–145. doi: 10.1007/s00412-006-0086-0. PubMed DOI

Traut W., Vogel H., Glöckner G., Hartmann E., Heckel D.G. High-throughput sequencing of a single chromosome: A moth W chromosome. Chromosome Res. 2013;110:491–505. doi: 10.1007/s10577-013-9376-6. PubMed DOI

Yoshido A., Šíchová J., Kubíčková S., Marec F., Sahara K. Rapid turnover of the W chromosome in geographical populations of wild silkmoths, Samia cynthia ssp. Chromosome Res. 2013;21:149–164. doi: 10.1007/s10577-013-9344-1. PubMed DOI

Yoshido A., Marec F., Sahara K. The fate of W chromosomes in hybrids between wild silkmoths, Samia cynthia ssp.: No role in sex determination and reproduction. Heredity. 2016;116:424–433. doi: 10.1038/hdy.2015.110. PubMed DOI PMC

Mediouni J., Fuková I., Frydrychová R., Dhouibi M.H., Marec F. Karyotype, sex chromatin and sex chromosome differentiation in the carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae) Caryologia. 2004;57:184–194. doi: 10.1080/00087114.2004.10589391. DOI

Lockwood A.P.M. “Ringer” solutions and some notes on the physiological basis of their ionic composition. Comp. Biochem. Physiol. 1961;2:241–289. doi: 10.1016/0010-406X(61)90113-X. PubMed DOI

Kubickova S., Cernohorska H., Musilova P., Rubes J. The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res. 2002;10:571–577. doi: 10.1023/A:1020914702767. PubMed DOI

Drosopoulou E., Nakou I., Šíchová J., Kubíčková S., Marec F., Mavragani-Tsipidou P. Sex chromosomes and associated rDNA form a heterochromatic network in the polytene nuclei of Bactrocera oleae (Diptera: Tephritidae) Genetica. 2012;140:169–180. doi: 10.1007/s10709-012-9668-3. PubMed DOI

Sahara K., Marec F., Traut W. TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 1999;7:449–460. doi: 10.1023/A:1009297729547. PubMed DOI

Kato A., Albert P.S., Vega J.M., Bichler J.A. Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech. Histochem. 2006;81:71–78. doi: 10.1080/10520290600643677. PubMed DOI

Fuková I., Nguyen P., Marec F. Codling moth cytogenetics: Karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome. 2005;1092:1083–1092. doi: 10.1139/g05-063. PubMed DOI

Shibata F., Sahara K., Naito Y., Yasukochi Y. Reprobing multicolor FISH preparations in lepidopteran chromosome. Zool. Sci. 2009;26:187–190. doi: 10.2108/zsj.26.187. PubMed DOI

Carabajal Paladino L.Z., Nguyen P., Šíchová J., Marec F. Mapping of single-copy genes by TSA-FISH in the codling moth, Cydia pomonella. BMC Genet. 2014;15(Suppl. 2):S15. doi: 10.1186/1471-2156-15-S2-S15. PubMed DOI PMC

Regier J.C., Mitter C., Zwick A., Bazinet A.L., Cummings M.P., Kawahara A.Y., Sohn J.-C., Zwickl D.J., Cho S., Davis D.R., et al. A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies) PLoS ONE. 2013;8:e58568. doi: 10.1371/journal.pone.0058568. PubMed DOI PMC

Wahlberg N., Wheat C.W., Peña C. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths) PLoS ONE. 2013;8:e80875. doi: 10.1371/journal.pone.0080875. PubMed DOI PMC

GenBank. [(accessed on 12 March 2018)]; Available online: https://www.ncbi.nlm.nih.gov/

Õunap E., Viidalepp J., Truuverk A. Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): Integrating molecular data and traditional classifications. Syst. Entomol. 2016;41:824–843. doi: 10.1111/syen.12195. DOI

Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Eickbush T.H., Eickbush D.G. Finely orchestrated movements: Evolution of the ribosomal RNA genes. Genetics. 2007;175:477–485. doi: 10.1534/genetics.107.071399. PubMed DOI PMC

Skou P., Sihvonen P., Ennominae I. In: The Geometrid Moths of Europe. Hausmann A., editor. Volume 5. E. J. Brill; Leiden, The Netherlands: 2015. p. 657.

Õunap E., Javoiš J., Viidalepp J., Tammaru T. Phylogenetic relationships of selected European Ennominae (Lepidoptera: Geometridae) Eur. J. Entomol. 2011;108:267–273. doi: 10.14411/eje.2011.036. DOI

Sihvonen P., Mutanen M., Kaila L., Brehm G., Hausmann A., Staude H.S. Comprehensive molecular sampling yields a robust phylogeny for geometrid moths (Lepidoptera: Geometridae) PLoS ONE. 2011;6:e20356. doi: 10.1371/journal.pone.0020356. PubMed DOI PMC

Traut W., Mosbacher C. Geschlechtschromatin bei Lepidopteren. Chromosoma. 1968;25:343–356. doi: 10.1007/BF01183125. PubMed DOI

Sahara K., Marec F., Eickhoff U., Traut W. Moth sex chromatin probed by comparative genomic hybridization (CGH) Genome. 2003;46:339–342. doi: 10.1139/g03-003. PubMed DOI

Hallast P., Jobling M.A. The Y chromosomes of the great apes. Hum. Genet. 2017;136:511–528. doi: 10.1007/s00439-017-1769-8. PubMed DOI

Bachtrog D. Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 2013;14:113–124. doi: 10.1038/nrg3366. PubMed DOI PMC

Yazdi H.P., Ellegren H. Old but not (so) degenerated—Slow evolution of largely homomorphic sex chromosomes in ratites. Mol. Biol. Evol. 2014;31:1444–1453. doi: 10.1093/molbev/msu101. PubMed DOI

Ellegren H. Sex-chromosome evolution: Recent progress and the influence of male and female heterogamety. Nat. Rev. Genet. 2011;12:157–166. doi: 10.1038/nrg2948. PubMed DOI

Shetty S., Griffin D.K., Graves J.A.M. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res. 1999;7:289–295. doi: 10.1023/A:1009278914829. PubMed DOI

Nishida-Umehara C., Tsuda Y., Ishijima J., Ando J., Fujiwara A., Matsuda Y., Griffin D.K. The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosome Res. 2007;15:721–734. doi: 10.1007/s10577-007-1157-7. PubMed DOI

Mank J.E., Ellegren H. Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol. Evol. 2007;22:389–391. doi: 10.1016/j.tree.2007.05.003. PubMed DOI

Yano C.F., Poltronieri J., Bertollo L.A., Artoni R.F., Liehr T., Cioffi M.B. Chromosomal mapping of repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): Insights into the differentiation of the Z and W chromosomes. PLoS ONE. 2014;9:e90946. doi: 10.1371/journal.pone.0090946. PubMed DOI PMC

Yano C.F., Bertollo L.A.C., Liehr T., Troy W.P., Cioffi M.B. W chromosome dynamics in Triportheus species (Characiformes, Triportheidae): An ongoing process narrated by repetitive sequences. J. Hered. 2016;107:342–348. doi: 10.1093/jhered/esw021. PubMed DOI PMC

Mariguela T.C., Roxo F.F., Foresti F., Oliveira C. Phylogeny and biogeography of Triportheidae (Teleostei: Characiformes) based on molecular data. Mol. Phylogenet. Evol. 2016;96:130–139. doi: 10.1016/j.ympev.2015.11.018. PubMed DOI

Charlesworth D., Charlesworth B., Marais G. Steps in the evolution of heteromorphic sex chromosomes. Heredity. 2005;95:118–128. doi: 10.1038/sj.hdy.6800697. 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

Garrido-Ramos M. Satellite DNA: An evolving topic. Genes. 2017;8:230. doi: 10.3390/genes8090230. PubMed DOI PMC

López-Flores I., Garrido-Ramos M.A. The repetitive DNA content of eukaryotic genomes. Genome Dyn. 2012;7:1–28. PubMed

Talla V., Suh A., Kalsoom F., Dincă V., Vila R., Friberg M., Wiklund C., Backström N. Rapid increase in genome size as a consequence of transposable element hyperactivity in wood-white (Leptidea) butterflies. Genome Biol. Evol. 2017;9:2491–2505. doi: 10.1093/gbe/evx163. PubMed DOI PMC

Van’t Hof A.E., Marec F., Saccheri I.J., Brakefield P.M., Zwaan B.J. Cytogenetic characterization and AFLP-based genetic linkage mapping for the butterfly Bicyclus anynana, covering all 28 karyotyped chromosomes. PLoS ONE. 2008;3:e3882. doi: 10.1371/journal.pone.0003882. PubMed DOI PMC

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

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Zygosity-based sex determination in a butterfly drives hypervariability of Masculinizer

. 2024 May 03 ; 10 (18) : eadj6979. [epub] 20240503

The Role of Repetitive Sequences in Repatterning of Major Ribosomal DNA Clusters in Lepidoptera

. 2023 Jun 01 ; 15 (6) : .

Accumulation of retrotransposons contributes to W chromosome differentiation in the willow beauty Peribatodes rhomboidaria (Lepidoptera: Geometridae)

. 2023 Jan 11 ; 13 (1) : 534. [epub] 20230111

New cytogenetic data on Caryophyllaeus laticeps and Paracaryophyllaeus gotoi, parasites of evolutionary interest

. 2022 Jul ; 149 (8) : 1094-1105. [epub] 20220510

Degenerated, Undifferentiated, Rearranged, Lost: High Variability of Sex Chromosomes in Geometridae (Lepidoptera) Identified by Sex Chromatin

. 2021 Aug 28 ; 10 (9) : . [epub] 20210828

Large-scale comparative analysis of cytogenetic markers across Lepidoptera

. 2021 Jun 09 ; 11 (1) : 12214. [epub] 20210609

Molecular cytogenetic analysis of a triploid population of the human broad tapeworm, Dibothriocephalus latus (Diphyllobothriidea)

. 2021 Jun ; 148 (7) : 787-797. [epub] 20210308

Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest

. 2021 Apr ; 30 (2) : 188-209. [epub] 20201222

The Role of Satellite DNAs in Genome Architecture and Sex Chromosome Evolution in Crambidae Moths

. 2021 ; 12 () : 661417. [epub] 20210330

Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation

. 2020 Jul 24 ; 11 (8) : . [epub] 20200724

Chromosomal study of Khawia abbottinae (Cestoda: Caryophyllidea): karyotype and localization of telomeric and ribosomal sequences after fluorescence in situ hybridization (FISH)

. 2019 Oct ; 118 (10) : 2789-2800. [epub] 20190904

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

. 2019 ; 10 () : 678. [epub] 20190802

Deciphering the Origin and Evolution of the X1X2Y System in Two Closely-Related Oplegnathus Species (Oplegnathidae and Centrarchiformes)

. 2019 Jul 22 ; 20 (14) : . [epub] 20190722

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace