Spiders are an intriguing model to analyse sex chromosome evolution because of their peculiar multiple X chromosome systems. Y chromosomes were considered rare in this group, arising after neo-sex chromosome formation by X chromosome-autosome rearrangements. However, recent findings suggest that Y chromosomes are more common in spiders than previously thought. Besides neo-sex chromosomes, they are also involved in the ancient X1X2Y system of haplogyne spiders, whose origin is unknown. Furthermore, spiders seem to exhibit obligatorily one or two pairs of cryptic homomorphic XY chromosomes (further cryptic sex chromosome pairs, CSCPs), which could represent the ancestral spider sex chromosomes. Here, we analyse the molecular differentiation of particular types of spider Y chromosomes in a representative set of ten species by comparative genomic hybridisation (CGH). We found a high Y chromosome differentiation in haplogyne species with X1X2Y system except for Loxosceles spp. CSCP chromosomes exhibited generally low differentiation. Possible mechanisms and factors behind the observed patterns are discussed. The presence of autosomal regions marked predominantly or exclusively with the male or female probe was also recorded. We attribute this pattern to intraspecific variability in the copy number and distribution of certain repetitive DNAs in spider genomes, pointing thus to the limits of CGH in this arachnid group. In addition, we confirmed nonrandom association of chromosomes belonging to particular CSCPs at spermatogonial mitosis and spermatocyte meiosis and their association with multiple Xs throughout meiosis. Taken together, our data suggest diverse evolutionary pathways of molecular differentiation in different types of spider Y chromosomes.

Biology Centre of the Czech Academy of Sciences Institute of Entomology Branišovská 31 370 05 České Budějovice Czech Republic

Department of Molecular Biology and Genetics Faculty of Science University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 128 44 Prague Czech Republic

Laboratory of Arachnid Cytogenetics Department of Genetics and Microbiology Faculty of Science Charles University Viničná 5 128 44 Prague Czech Republic

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 277 21 Liběchov Czech Republic

Zobrazit více v PubMed

Ironside J.E. No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution. BioEssays. 2010;32:718–726. doi: 10.1002/bies.200900124. 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

Grossen C., Neuenschwander S., Perrin N. The evolution of XY recombination: Sexually antagonistic selection versus deleterious mutation load. Evolution. 2012;66:3155–3166. doi: 10.1111/j.1558-5646.2012.01661.x. PubMed DOI

Mank J.E. Sex chromosome dosage compensation: Definitely not for everyone. Trends Genet. 2013;29:677–683. doi: 10.1016/j.tig.2013.07.005. 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

Vicoso B., Bachtrog D. Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature. 2013;499:332–335. doi: 10.1038/nature12235. 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

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

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

Tomaszkiewicz M., Medvedev P., Makova K.D. Y and W chromosome assemblies: Approaches and discoveries. Trends Genet. 2017;33:266–282. doi: 10.1016/j.tig.2017.01.008. PubMed DOI

Cavoto E., Neuenschwander S., Goudet J., Perrin N. Sex-antagonistic genes, XY recombination and feminized Y chromosomes. J. Evol. Biol. 2018;31:416–427. doi: 10.1111/jeb.13235. PubMed DOI

Ohno S. Sex Chromosomes and Sex-Linked Genes. Springer; New York, NY, USA: 1967. pp. 1–192.

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

Wright A.E., Dean R., Zimmer F., Mank J.E. How to make a sex chromosome. Nat. Commun. 2016;7:12087. doi: 10.1038/ncomms12087. PubMed DOI PMC

Bergero R., Charlesworth D. The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 2009;24:94–102. doi: 10.1016/j.tree.2008.09.010. PubMed 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

Blackmon H., Ross L., Bachtrog D. Sex determination, sex chromosomes, and karyotype evolution in insects. J. Hered. 2017;108:78–93. doi: 10.1093/jhered/esw047. PubMed DOI PMC

Král J. Evolution of multiple sex chromosomes in the spider genus Malthonica (Araneae: Agelenidae) indicates unique structure of the spider sex chromosome systems. Chromosome Res. 2007;15:863–879. doi: 10.1007/s10577-007-1169-3. PubMed DOI

Král J., Kořínková T., Forman M., Krkavcová L. Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders. Cytogenet. Genome Res. 2011;133:43–66. doi: 10.1159/000323497. PubMed DOI

Araujo D., Schneider M.C., Paula-Neto E., Cella D.M. Sex chromosomes and meiosis in spiders: A review. In: Swan A., editor. Meiosis—Molecular Mechanisms and Cytogenetic Diversity. Volume 5. InTechOpen; Rieka, Croatia: 2012. pp. 87–108.

Král J., Kořínková T., Krkavcová L., Musilová J., Forman M., Ávila Herrera I.M., Haddad C.R., Vítková M., Henriques S., Palacios Vargas J.G., et al. Evolution of karyotype, sex chromosomes, and meiosis in mygalomorph spiders (Araneae: Mygalomorphae) Biol. J. Linn. Soc. 2013;109:377–408. doi: 10.1111/bij.12056. DOI

Kořínková T., Král J. Karyotypes, sex chromosomes, and meiotic division in spiders. In: Nentwig W., editor. Spider Ecophysiology. 1st ed. Springer; Berlin, Germany: 2013. pp. 159–169. DOI

World Spider Catalog. [(accessed on 24 May 2020)]; Available online: https://wsc.nmbe.ch/

Coddington J.A., Levi H.W. Systematics and evolution of spiders (Araneae) Annu. Rev. Ecol. Syst. 1991;22:565–592. doi: 10.1146/annurev.es.22.110191.003025. DOI

Coddington J.A. Phylogeny and classification of spiders. In: Ubick D., Paquin P., Cushing P.E., Roth V., editors. Spiders of North America: An Identification Manual. American Arachnological Society; San Francisco, CA, USA: 2005. pp. 18–24.

Suzuki S. Cytological studies in spiders. III. Studies on the chromosomes of fifty-seven species of spiders belonging to seventeen families with general considerations on chromosomal evolution. J. Sci. Hiroshima Univ. B. 1954;15:23–136.

White M.J.D. Animal Cytology and Evolution. 3rd ed. Cambridge University Press; London, UK: 1973. pp. 1–468.

Palacios-Gimenez O.M., Cabral-de Mello D.C. Repetitive DNA chromosomal organization in the cricket Cycloptiloides americanus: A case of the unusual X1X20 sex chromosome system in Orthoptera. Mol. Genet. Genomics. 2015;290:623–631. doi: 10.1007/s00438-014-0947-9. PubMed DOI

Postiglioni A., Brum-Zorrilla M. Karyological studies on Uruguayan spiders II. Sex chromosomes in spiders of the genus Lycosa (Araneae-Lycosidae) Genetica. 1981;56:47–53. doi: 10.1007/BF00126929. DOI

Maddison W.P. XXXY sex chromosomes in males of the jumping spider genus Pellenes (Araneae: Salticidae) Chromosoma. 1982;85:23–37. doi: 10.1007/BF00344592. DOI

Král J., Musilová J., Šťáhlavský F., Řezáč M., Akan Z., Edwards R.L., Coyle F.A., Almerje C.R. Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae) Chromosome Res. 2006;14:859–880. doi: 10.1007/s10577-006-1095-9. PubMed DOI

Řezáč M., Král J., Musilová J., Pekár S. Unusual karyotype diversity in the European spiders of the genus Atypus (Araneae: Atypidae) Hereditas. 2006;143:123–129. doi: 10.1111/j.2006.0018-0661.01949.x. PubMed DOI

Sharp H.E., Rowell D.M. Unprecedented chromosomal diversity and behaviour modify linkage patterns and speciation potential: Structural heterozygosity in an Australian spider. J. Evol. Biol. 2007;20:2427–2439. doi: 10.1111/j.1420-9101.2007.01395.x. PubMed DOI

Maddison W.P., Leduc-Robert G. Multiple origins of sex chromosome fusions correlated with chiasma localization in Habronattus jumping spiders (Araneae: Salticidae) Evolution. 2013;67:2258–2272. doi: 10.1111/evo.12109. PubMed DOI PMC

Maddison W.P., Maddison D.R., Derkarabetian S., Hedin M. Sitticine jumping spiders: Phylogeny, classification, and chromosomes (Araneae, Salticidae, Sitticini) ZooKeys. 2020;925:1–54. doi: 10.3897/zookeys.925.39691. PubMed DOI PMC

Silva R.W., Klisiowicz D.D.R., Cella D.M., Mangili O.C., Sbalqueiro I.J. Differential distribution of constitutive heterochromatin in two species of brown spider: Loxosceles intermedia and L. laeta (Araneae, Sicariidae), from the metropolitan region of Curitiba, PR (Brasil) Acta Biol. Parana. 2002;31:123–136.

Král J., Forman M., Kořínková T., Reyes Lerma A.C., Haddad C.R., Musilová J., Řezáč M., Ávila Herrera I., Thakur S., Dippenaar-Schoeman A.S., et al. Insights into the karyotype and genome evolution of haplogyne spiders indicate a polyploid origin of lineage with holokinetic chromosomes. Sci. Rep. 2019;9:3001. doi: 10.1038/s41598-019-39034-3. PubMed DOI PMC

Araujo D., Schneider M.C., Zacaro A.A., de Oliveira E.G., Martins R., Brescovit A.D., Knysak I., Cella D.M. Venomous Loxosceles species (Araneae, Haplogynae, Sicariidae) from Brazil: 2n♂ = 23 and X1X2Y sex chromosome system as shared characteristics. Zoolog. Sci. 2020;37:128–139. doi: 10.2108/zs190128. PubMed DOI

Paula-Neto E., Cella D.M., Araújo D., Brescovit A.D., Schneider M.C. Comparative cytogenetic analysis among filistatid spiders (Araneomorphae: Haplogynae) J. Arachnol. 2017;45:123–128. doi: 10.1636/M14-69.1. DOI

Cordellier M., Schneider J.M., Uhl G., Posnien N. Sex differences in spiders: From phenotype to genomics. Dev. Genes Evol. 2020;230:155–172. doi: 10.1007/s00427-020-00657-6. PubMed DOI PMC

Sheffer M.M., Hoppe A., Krehenwinkel H., Uhl G., Kuss A.W., Jensen L., Jensen C., Gillespie R.G., Hoff K.J., Prost S. Chromosome-level reference genome of the European wasp spider Argiope bruennichi: A resource for studies on range expansion and evolutionary adaptation. bioRxiv. 2020 doi: 10.1101/2020.05.21.103564. PubMed DOI PMC

Bechsagaard J., Schou M.F., Vanthournout B., Hendrickx F., Knudsen B., Settepani V., Schierup M.H., Bilde T. Evidence for faster X chromosome evolution in spiders. Mol. Biol. Evol. 2019;36:1281–1293. doi: 10.1093/molbev/msz074. PubMed DOI PMC

Traut W., Winking H. Meiotic chromosomes and stages of sex chromosome evolution in fish: Zebrafish, platyfish and guppy. Chromosome Res. 2001;9:659–672. doi: 10.1023/A:1012956324417. 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

Pokorná M., Rens W., Rovatsos M., Kratochvíl L. A ZZ/ZW sex chromosome system in the thick-tailed gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a member of the ancient gecko lineage. Cytogenet. Genome Res. 2014;142:190–196. doi: 10.1159/000358847. PubMed DOI

Šíchová J., Voleníková A., Dincă V., Nguyen P., Vila R., Sahara K., Marec F. Dynamic karyotype evolution and unique sex determinatin systems in Leptidea wood white butterflies. BMC Evol. Biol. 2015;15:1–16. doi: 10.1186/s12862-015-0375-4. PubMed DOI PMC

Altmanová M., Rovatsos M., Kratochvíl L., Johnson Pokorná M. Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae) Biol. J. Linn. Soc. 2016;118:618–633. doi: 10.1111/bij.12751. DOI

Montiel E.E., Badenhorst D., Tamplin J., Burke R.L., Valenzuela N. Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma. 2017;126:105–113. doi: 10.1007/s00412-016-0576-7. PubMed DOI

Yano C.F., Bertollo L.A.C., Ezaz T., Trifonov V., Sember A., Liehr T., Cioffi M.B. Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae) Heredity. 2017;118:276–283. doi: 10.1038/hdy.2016.83. PubMed DOI PMC

Sember A., Bertollo L.A.C., Yano C.F., Hatanaka T., Ráb P., de Oliveira E.A., Cioffi M.B. Sex chromosome evolution and genomic divergence in the fish Hoplias malabaricus (Characiformes, Erythrinidae) Front. Genet. 2018;9:1–12. doi: 10.3389/fgene.2018.00071. PubMed DOI PMC

Zrzavá M., Hladová I., Dalíková M., Šíchová J., Õunap E., Kubíčková S., Marec F. Sex chromosomes of the iconic moth Abraxas grossulariata (Lepidoptera, Geometridae) and its congener A. sylvata. Genes. 2018;9:279. doi: 10.3390/genes9060279. PubMed DOI PMC

Moraes R.L., Sember A., Bertollo L.A.C., de Oliveira E.A., Ráb P., Hatanaka T., Marinho M.M.F., Liehr T., Al-Rikabi A.B.H., Feldberg E., et al. Comparative cytogenetics and neo-Y formation in small-sized fish species of the genus Pyrrhulina (Characiformes, Lebiasinidae) Front. Genet. 2019;10:1–13. doi: 10.3389/fgene.2019.00678. PubMed DOI PMC

Dolejš P., Kořínková T., Musilová J., Opatová V., Kubcová L., Buchar J., Král J. Karyotypes of central European spiders of the genera Arctosa, Tricca, and Xerolycosa (Araneae: Lycosidae) Eur. J. Entomol. 2011;108:1–16. doi: 10.14411/eje.2011.001. DOI

Winnepenninckx B., Backeljau T., De Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993;9:407. doi: 10.1016/0168-9525(93)90102-N. PubMed DOI

Kubíčková S., Černohorská H., Musilová P., Rubeš J. The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Vet. Res. 2002;10:571–577. doi: 10.1023/A:1020914702767. PubMed DOI

Britten R.J., Graham D.E., Neufeld B.R. Analysis of repeating DNA sequences by reassociation. Methods Enzymol. 1974;29:363–418. doi: 10.1016/0076-6879(74)29033-5. PubMed DOI

Peterson D.G., Pearson W.R., Stack S.M. Characterization of the tomato (Lycopsersicon esculentum) genome using in vitro and in situ DNA reassociation. Genome. 1998;41:346–356. doi: 10.1139/g98-025. DOI

Zwick M.S., Hanson R.E., McKnight T.D., Islam-Faridi M.N., Stelly D.M., Wing R.A., Price H.J. A rapid procedure for the isolation of Cot-1 DNA from plants. Genome. 1997;40:138–142. doi: 10.1139/g97-020. PubMed DOI

Traut W., Eickhoff U., Schorch J.C. Identification and analysis of sex chromosomes by comparative genomic hybridization (CGH) Methods Cell Sci. 2001;23:157–163. doi: 10.1023/A:1013138925996. PubMed DOI

Symonová R., Sember A., Majtánová Z., Ráb P. Characterization of fish genomes by GISH and CGH. In: Ozouf-Costaz C., Pisano E., Foresti F., de Almeida L.F., editors. Fish Cytogenetic Techniques. 1st ed. CRC Press; Cleveland, OH, USA: 2015. pp. 118–131. DOI

Sember A., Bohlen J., Šlechtová V., Altmanová M., Symonová R., Ráb P. Karyotype differentiation in 19 species of river loach fishes (Nemacheilidae, Teleostei): Extensive variability associated with rDNA and heterochromatin distribution and its phylogenetic and ecological interpretation. BMC Evol. Biol. 2015;15:251. doi: 10.1186/s12862-015-0532-9. PubMed DOI PMC

Levan A., Fredga K., Sandberg A.A. Nomenclature for centromeric position on chromosomes. Hereditas. 1964;52:201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x. DOI

Wheeler W.C., Coddington J.A., Crowley L.M., Dimitrov D., Goloboff P.A., Griswold C.E., Hormiga G., Prendini L., Ramírez M.J., Sierwald P., et al. The spider tree of life: Phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics. 2017;33:574–616. doi: 10.1111/cla.12182. PubMed DOI

Lüddecke T., Krehenwinkel H., Canning G., Glaw F., Longhorn S.J., Tänzler R., Wendt I., Vences M. Discovering the silk road: Nuclear and mitochondrial sequence data resolve the phylogenetic relationships among theraphosid spider subfamilies. Mol. Phylogenet. Evol. 2018;119:63–70. doi: 10.1016/j.ympev.2017.10.015. PubMed DOI

Fernandez R., Kallal R.J., Dimitrov D., Ballesteros J.A., Arnedo M.A., Giribet G., Hormiga G. Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life. Curr. Biol. 2018;28:1489–1497. doi: 10.1016/j.cub.2018.03.064. PubMed DOI

Chirino M.G., Fourastie M.F., Centeno N.D., Bressa M.J. Unusual chromosome polymorphism and heterochromatin variation in the Argentinean population of the necrophagous fly Lucilia sericata (Diptera: Calliphoridae), comparison with other populations and evolutionary aspects. Eur. J. Entomol. 2020;117:295–301. doi: 10.14411/eje.2020.034. DOI

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

Fotsig S.F., Margoliash J., Wang C., Saini S., Yanicky R., Shleizer-Burko S., Goren A., Gymrek M.T. The impact of short tandem repeat variation on gene expression. Nat. Genet. 2019;51:1652–1659. doi: 10.1038/s41588-019-0521-9. PubMed DOI PMC

Ananiev E.V., Chamberlin M.A., Klaiber J., Svitashev S. Microsatellite megatracts in the maize (Zea mays L.) genome. Genome. 2005;48:1061–1069. doi: 10.1139/g05-061. PubMed DOI

Hughes J.F., Skaletsky H., Koutseva N., Pyntikova T., Page D.C. Sex chromosome-to-autosome transposition events counter Y-chromosome gene loss in mammals. Genome Biol. 2015;16:104. doi: 10.1186/s13059-015-0667-4. PubMed DOI PMC

Murata C., Kuroki Y., Imoto I., Kuroiwa A. Ancestral Y-linked genes were maintained by translocation to the X and Y chromosomes fused to an autosomal pair in the Okinawa spiny rat Tokudaia muenninki. Chromosome Res. 2016;24:407–419. doi: 10.1007/s10577-016-9531-y. PubMed DOI

Tobler R., Nolte V., Schlötterer C. High rate of translocation-based gene birth on the Drosophila Y chromosome. Proc. Natl. Acad. Sci. USA. 2017;114:201706502. doi: 10.1073/pnas.1706502114. PubMed DOI PMC

Willems T., Gymrek M., Poznik G.D., Tyler-Smith C. The 1000 Genomes Project Chromosome Y Group, Erlich, Y. 2016. Population-scale sequencing data enable precise estimates of Y-STR mutation rates. Am. J. Hum. Genet. 2016;98:919–933. doi: 10.1016/j.ajhg.2016.04.001. PubMed DOI PMC

Jablonka E., Lamb M.J. Meiotic pairing constraints and the activity of sex chromosomes. J. Theor. Biol. 1988;133:23–36. doi: 10.1016/S0022-5193(88)80022-5. PubMed DOI

McKee B.D., Handel M.A. Sex chromosomes, recombination, and chromatin conformation. Chromosoma. 1993;102:71–80. doi: 10.1007/BF00356023. PubMed DOI

Noronha R.C.R., Nagamachi C.Y., O’Brien P.C.M., Ferguson-Smith M.A., Pieczarka J.C. Neo-XY body: An analysis of XY1Y2 meiotic behavior in Carollia (Chiroptera, Phyllostomidae) by chromosome painting. Cytogenet. Genome Res. 2009;124:37–43. doi: 10.1159/000200086. PubMed DOI

Garrison N.L., Rodriguez J., Agnarsson I., Coddington J.A., Griswold C.E., Hamilton C.A., Hedin M., Kocot K.M., Ledford J.M., Bond J.E. Spider phylogenomics: Untangling the Spider Tree of Life. PeerJ. 2016;4:e1719. doi: 10.7717/peerj.1719. PubMed DOI PMC

Silva D. Estudio cariotípico de Loxosceles laeta (Araneae: Loxoscelidae) Rev. Perúana Entomol. 1988;31:9–12.

Sumner A.T. Chromosome Banding. Unwin Hyman; London, UK: 1990.

Matsunaga S. Junk DNA promotes sex chromosome evolution. Heredity. 2009;102:525–526. doi: 10.1038/hdy.2009.36. PubMed DOI

Moreira-Filho O., Bertollo L.A.C., Galetti P.M., Jr. Distribution of sex chromosome mechanisms in neotropical fish and description of a ZZ/ZW system in Parodon hilarii (Parodontidae) Caryologia. 1993;46:115–125. doi: 10.1080/00087114.1993.10797253. DOI

Shibata F., Hizume M., Kuroki Y. Chromosome painting of Y chromosomes and isolation of a Y chromosome-specific repetitive sequence in the dioecious plant Rumex acetosa. Chromosoma. 1999;108:266–270. doi: 10.1007/s004120050377. PubMed DOI

Schmid M., Feichtinger W., Steinlein C., Rupprecht T., Haaf T., Kaiser H. Chromosome banding in Amphibia. XXIII. Giant W sex chromosomes and extremely small genomes in Eleutherodactylus euphronides and Eleutherodactylus shrevei (Anura, Leptodactylidae) Cytogenet. Genome Res. 2002;97:81–94. doi: 10.1159/000064055. PubMed DOI

De Oliveira R.R., Feldberg E., Dos Anjos M.B., Zuanon J. Karyotype characterization and ZZ/ZW sex chromosome heteromorphism in two species of the catfish genus Ancistrus Kner, 1854 (Siluriformes: Loricariidae) from the Amazon basin. Neotrop. Ichthyol. 2007;5:301–306. doi: 10.1590/S1679-62252007000300010. DOI

Kejnovský E., Hobza R., Čermák T., Kubát Z., Vyskot B. The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity. 2009;102:533–541. doi: 10.1038/hdy.2009.17. PubMed DOI

Sousa A., Fuchs J., Renner S.S. Molecular cytogenetics (FISH, GISH) of Coccinia grandis: A ca. 3 myr-old species of Cucurbitaceae with the largest Y/autosome divergence in flowering plants. Cytogenet. Genome Res. 2013;139:107–118. doi: 10.1159/000345370. PubMed DOI

Poltronieri J., Marquioni V., Bertollo L.A.C., Kejnovský E., Molina W.F., Liehr T., Cioffi M.B. Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): Unequal accumulation on the W chromosomes. Cytogenet. Genome Res. 2013;142:40–45. doi: 10.1159/000355908. PubMed DOI

Viana P.F., Ezaz T., Marajó L., Ferreira M., Zuanon J., Cioffi M.B., Bertollo L.A.C., Gross M.C., Feldberg E. Genomic organization of repetitive DNAs and differentiation of an XX/XY sex chromosome system in the Amazonian puffer fish, Colomesus asellus (Tetraodontiformes) Cytogenet. Genome Res. 2017;153:96–104. doi: 10.1159/000484423. PubMed DOI

Wolf K.W. How meiotic cells deal with non-exchange chromosomes. BioEssays. 1994;16:107–114. doi: 10.1002/bies.950160207. PubMed DOI

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

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

Uno Y., Nishida C., Yoshimoto S., Ito M., Oshima Y., Yokoyama S., Nakamura M., Matsuda Y. Diversity in the origins of sex chromosomes in anurans inferred from comparative mapping of sexual differentiation genes for three species of the Raninae and Xenopodinae. Chromosome Res. 2008;16:999–1011. doi: 10.1007/s10577-008-1257-z. PubMed DOI

Green J.E., Dalíková M., Sahara K., Marec F., Akam M. XX/XY system of sex determination in the geophilomorph centipede Strigamia maritima. PLoS ONE. 2016;11:e0150292. doi: 10.1371/journal.pone.0150292. PubMed DOI PMC

Augstenová B., Johnson Pokorná M., Altmanová M., Frynta D., Rovatsos M., Kratochvíl L. ZW, XY, and yet ZW: Sex chromosome evolution in snakes even more complicated. Evolution. 2018;72:1701–1707. doi: 10.1111/evo.13543. PubMed DOI

Kato A., Vega J.M., Han F., Lamb J.C., Bircher J.A. Advances in plant chromosome identification and cytogenetic techniques. Curr. Opin. Plant. Biol. 2005;8:148–154. doi: 10.1016/j.pbi.2005.01.014. PubMed DOI

Markova M., Vyskot B. New horizons of genomic in situ hybridization. Cytogenet. Genome Res. 2010;126:368–375. doi: 10.1159/000275796. PubMed DOI

Lahn B.T., Page D.C. Four evolutionary strata on the human X chromosome. Science. 1999;286:964–967. doi: 10.1126/science.286.5441.964. PubMed DOI

Toder R., Wienberg J., Voullaire L., O’Brien P.C.M., Maccarone P., Marshall Graves J.A. Shared DNA sequences between the X and Y chromosomes in the tammar wallaby–Evidence for independent additions to eutherian and marsupial sex chromosomes. Chromosoma. 1997;106:94–98. doi: 10.1007/s004120050228. PubMed DOI

Lisachov A.P., Makunin A.I., Giovannotti M., Pereira J.C., Druzhkova A.S., Caputo Barucchi V., Ferguson-Smith M.A., Trifonov V.A. Genetic content of the neo-sex chromosomes in Ctenonotus and Norops (Squamata, Actyloidae) and degeneration of the Y chromosome as revealed by high-throughput sequencing of individual chromosomes. Cytogenet. Genome Res. 2019;157:115–122. doi: 10.1159/000497091. PubMed DOI

Blackmon H., Demuth J.P. The fragile Y hypothesis: Y chromosome aneuploidy as a selective pressure in sex chromosome and meiotic mechanism evolution. BioEssays. 2015;37:942–950. doi: 10.1002/bies.201500040. PubMed DOI

Rovatsos M., Farkačová K., Altmanová M., Johnson Pokorná M., Kratochvíl L. The rise and fall of differentiated sex chromosomes in geckos. Mol. Ecol. 2019;28:3042–3052. doi: 10.1111/mec.15126. 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

Mongue A.J., Nguyen P., Voleníková A., Walters J.R. Neo-sex chromosomes in the monarch butterfly, Danaus plexippus. G3 (Bethesda) 2017;7:g3.300187.2017. doi: 10.1534/g3.117.300187. PubMed DOI PMC

Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994;371:215–220. doi: 10.1038/371215a0. PubMed DOI

Ávila Herrera I.M., Král J., Pastuchová M., Forman M., Musilová J., Kořínková T., Šťáhlavský F., Zrzavá M., Nguyen P., Koubová M., et al. Evolutionary pattern of karyotypes, nucleolus organizer regions, sex chromosomes, and meiosis in pholcid spiders (Araneae: Pholcidae): Implications for reconstructing karyotype evolution of araneomorph spiders. BMC Evol. Biol. submitted.

Araujo D., Schneider M.C., Paula-Neto E., Cella D.M. The Spider Cytogenetic Database. [(accessed on 17 June 2020)]; Available online: www.arthropodacytogenetics.bio.br/spiderdatabase.

Cuñado N., Navajas-Pérez R., de la Herrán R., Rejón C.R., Rejón M.R., Santos J.L., Garrido-Ramos M.A. The evolution of sex chromosomes in the genus Rumex (Polygonaceae): Identification of a new species with heteromorphic sex chromosomes. Chromosome Res. 2007;15:825–832. doi: 10.1007/s10577-007-1166-6. PubMed DOI

Mariotti B., Manzano S., Kejnovský E., Vyskot B., Jamilena M. Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes. Mol. Genet. Genom. 2009;281:249–259. doi: 10.1007/s00438-008-0405-7. 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

Jetybayev I.Y., Bugrov A.G., Ünal M., Buleu O.G., Rubtsov N.B. Molecular cytogenetic analysis reveals the existence of two independent neo-XY sex chromosome systems in Anatolian Pamphagidae grasshoppers. BMC Evol. Biol. 2017;17:20. doi: 10.1186/s12862-016-0868-9. PubMed DOI PMC

Palacios-Gimenez O.M., Dias G.B., de Lima L.G., Kuhn G.C.E.S., Ramos É., Martins C., Cabral-de-Mello D.C. High-throughput analysis of the satellitome revealed enormous diversity of satellite DNAs in the neo-Y chromosome of the cricket Eneoptera surinamensis. Sci. Rep. 2017;7:6422. doi: 10.1038/s41598-017-06822-8. PubMed DOI PMC

Gazoni T., Haddad C.F.B., Narimatsu H., Cabral-de-Mello D.C., Lyra M.L., Parise-Maltempi P.P. More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma. 2018;127:269–278. doi: 10.1007/s00412-018-0663-z. PubMed DOI

Xu D., Sember A., Zhu Q., Oliveira E.A., Liehr T., Al-Rikabi A.B.H., Xiao Z., Song H., Cioffi M.B. Deciphering the origin and evolution of the X1X2Y system in two closely-related Oplegnathus species (Oplegnathidae and Centrarchiformes) Int. J. Mol. Sci. 2019;20:3571. doi: 10.3390/ijms20143571. PubMed DOI PMC

Advances in Understanding the Karyotype Evolution of Tetrapulmonata and Two Other Arachnid Taxa, Ricinulei and Solifugae

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

Karyotype differentiation and male meiosis in European clades of the spider genus Pholcus (Araneae, Pholcidae)

Atypus karschi Dönitz, 1887 (Araneae: Atypidae): An Asian purse-web spider established in Pennsylvania, USA

Insights into the Karyotype Evolution of Charinidae, the Early-Diverging Clade of Whip Spiders (Arachnida: Amblypygi)