Madagascar Leaf-Tail Geckos (Uroplatus spp.) Share Independently Evolved Differentiated ZZ/ZW Sex Chromosomes
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36672195
PubMed Central
PMC9856856
DOI
10.3390/cells12020260
PII: cells12020260
Knihovny.cz E-zdroje
- Klíčová slova
- DNA-seq, cytogenetics, evolution, genomics, qPCR, reptiles, sex chromosomes, sex determination,
- MeSH
- fylogeneze MeSH
- ještěři * genetika MeSH
- pohlavní chromozomy genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Madagaskar MeSH
Geckos are an excellent group to study the evolution of sex determination, as they possess a remarkable variability ranging from a complete absence of sex chromosomes to highly differentiated sex chromosomes. We explored sex determination in the Madagascar leaf-tail geckos of the genus Uroplatus. The cytogenetic analyses revealed highly heterochromatic W chromosomes in all three examined species (Uroplatus henkeli, U. alluaudi, U. sikorae). The comparative gene coverage analysis between sexes in U. henkeli uncovered an extensive Z-specific region, with a gene content shared with the chicken chromosomes 8, 20, 26 and 28. The genomic region homologous to chicken chromosome 28 has been independently co-opted for the role of sex chromosomes in several vertebrate lineages, including monitors, beaded lizards and monotremes, perhaps because it contains the amh gene, whose homologs were repeatedly recruited as a sex-determining locus. We demonstrate that all tested species of leaf-tail geckos share homologous sex chromosomes despite the differences in shape and size of their W chromosomes, which are not homologous to the sex chromosomes of other closely related genera. The rather old (at least 40 million years), highly differentiated sex chromosomes of Uroplatus geckos can serve as a great system to study the convergence of sex chromosomes evolved from the same genomic region.
Zobrazit více v PubMed
Bull J.J. Evolution of Sex Determining Mechanisms. Benjamin/Cumming; Menlo Park, CA, USA: 1983.
Capel B. Current Topics in Developmental Biology. Volume 134 Elsevier; Amsterdam, The Netherlands: New York, NY, USA: 2019. Sex determination in vertebrates.
Kratochvíl L., Stöck M., Rovatsos M., Bullejos M., Herpin A., Jeffries D.L., Peichel C.L., Perrin N., Valenzuela N., Johnson Pokorná M. Expanding the classical paradigm: What we have learnt from vertebrates about sex chromosome evolution. Philos. Trans. R. Soc. B. 2021;376:20200097. doi: 10.1098/rstb.2020.0097. PubMed DOI PMC
Stöck M., Kratochvíl L., Kuhl H., Rovatsos M., Evans B.J., Suh A., Valenzuela N., Veyrunes F., Zhou Q., Gamble T., et al. A brief review of vertebrate sex evolution with a pledge for integrative research: Towards ‘sexomics’. Philos. Trans. R. Soc. B. 2021;376:20200426. doi: 10.1098/rstb.2020.0426. PubMed DOI PMC
Cortez D., Marin R., Toledo-Flores D., Froidevaux L., Liechti A., Waters P.D., Grützner F., Kaessmann H. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508:488–493. doi: 10.1038/nature13151. PubMed DOI
Zhou Q., Zhang J., Bachtrog D., An N., Huang Q., Jarvis E.D., Gilbert M.T.P., Zhang G. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science. 2014;346:1246338. doi: 10.1126/science.1246338. PubMed DOI PMC
Rovatsos M., Pokorná M., Altmanová M., Kratochvíl L. Cretaceous park of sex determination: Sex chromosomes are conserved across iguanas. Biol. Lett. 2014;10:20131093. doi: 10.1098/rsbl.2013.1093. PubMed DOI PMC
Rovatsos M., Vukić J., Lymberakis P., Kratochvíl L. Evolutionary stability of sex chromosomes in snakes. Proc. R. Soc. B. 2015;282:20151992. doi: 10.1098/rspb.2015.1992. PubMed DOI PMC
Iannucci A., Altmanová M., Ciofi C., Ferguson-Smith M., Milan M., Pereira J.C., Pether J., Rehák I., Rovatsos M., Stanyon R., et al. Conserved sex chromosomes and karyotype evolution in monitor lizards (Varanidae) Heredity. 2019;123:215–227. doi: 10.1038/s41437-018-0179-6. PubMed DOI PMC
Kostmann A., Kratochvíl L., Rovatsos M. Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proc. R. Soc. B. 2021;288:20202139. doi: 10.1098/rspb.2020.2139. PubMed DOI PMC
Rovatsos M., Vukić J., Mrugała A., Suwala G., Lymberakis P., Kratochvíl L. Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards. Sci. Rep. 2019;9:7832. doi: 10.1038/s41598-019-44192-5. PubMed DOI PMC
Pennell M.W., Mank J.E., Peichel C.L. Transitions in sex determination and sex chromosomes across vertebrate species. Mol. Ecol. 2018;27:3950–3963. doi: 10.1111/mec.14540. PubMed DOI PMC
Sember A., Nguyen P., Perez M.F., Altmanová M., Ráb P., Cioffi M.B. Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: State of the art and future challenges. Philos. Trans. R. Soc. B. 2021;376:20200098. doi: 10.1098/rstb.2020.0098. PubMed DOI PMC
Kuhl H., Guiguen Y., Höhne C., Kreuz E., Du K., Klopp C., Lopez-Roques C., Yebra-Pimentel E.S., Ciorpac M., Gessner J., et al. A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes. Philos. Trans. R. Soc. B. 2021;376:20200089. doi: 10.1098/rstb.2020.0089. PubMed DOI PMC
Jeffries D.L., Lavanchy G., Sermier R., Sredl M.J., Miura I., Borzée A., Barrow L.N., Canestrelli D., Crochet P.-A., Dufresnes C., et al. A rapid rate of sex-chromosome turnover and non-random transitions in true frogs. Nat. Commun. 2018;9:4088. doi: 10.1038/s41467-018-06517-2. PubMed DOI PMC
Bertho S., Herpin A., Schartl M., Guiguen Y. Lessons from an unusual vertebrate sex-determining gene. Philos. Trans. R. Soc. B. 2021;376:20200092. doi: 10.1098/rstb.2020.0092. PubMed DOI PMC
Kabir A., Ieda R., Hosoya S., Fujikawa D., Atsumi K., Tajima S., Nozawa A., Koyama T., Hirase S., Nakamura O., et al. Repeated translocation of a supergene underlying rapid sex chromosome turnover in Takifugu pufferfish. Proc. Natl. Acad. Sci. USA. 2022;119:e2121469119. doi: 10.1073/pnas.2121469119. PubMed DOI PMC
Ross J.A., Urton J.R., Boland J., Shapiro M.D., Peichel C.L. Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae) PLoS Genet. 2009;5:e1000391. doi: 10.1371/journal.pgen.1000391. PubMed DOI PMC
Myosho T., Takehana Y., Hamaguchi S., Sakaizumi M. Turnover of sex chromosomes in celebensis group medaka fishes. G3. 2015;5:2685–2691. doi: 10.1534/g3.115.021543. PubMed DOI PMC
El Taher A., Ronco F., Matschiner M., Salzburger W., Böhne A. Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes. Sci. Adv. 2021;7:eabe8215. doi: 10.1126/sciadv.abe8215. PubMed DOI PMC
Augstenová B., Pensabene E., Veselý M., Kratochvíl L., Rovatsos M. Are geckos special in sex determination? Independently evolved differentiated ZZ/ZW sex chromosomes in carphodactylid geckos. Genome Biol. Evol. 2021;13:evab119. doi: 10.1093/gbe/evab119. PubMed DOI PMC
Gamble T. A review of sex determining mechanisms in geckos (Gekkota: Squamata) Sex. Dev. 2010;4:88–103. doi: 10.1159/000289578. PubMed DOI PMC
Gamble T., Coryell J., Ezaz T., Lynch J., Scantlebury D.P., Zarkower D. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 2015;32:1296–1309. doi: 10.1093/molbev/msv023. PubMed DOI
Uetz P., Freed P., Aguilar R., Hošek J., editors. The Reptile Database. [(accessed on 23 May 2021)]. Available online: https://www.reptile-database.org.
Pyron R.A., Burbrink F.T., Wiens J.J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 2013;13:93. doi: 10.1186/1471-2148-13-93. PubMed DOI PMC
Pokorná M., Kratochvíl L. Phylogeny of sex-determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 2009;156:168–183. doi: 10.1111/j.1096-3642.2008.00481.x. DOI
Johnson Pokorná M., Kratochvíl L. What was the ancestral sex-determining mechanism in amniote vertebrates? Biol. Rev. 2016;91:1–12. doi: 10.1111/brv.12156. PubMed DOI
Pensabene E., Kratochvíl L., Rovatsos M. Independent evolution of sex chromosomes in eublepharid geckos, a lineage with environmental and genotypic sex determination. Life. 2020;10:342. doi: 10.3390/life10120342. PubMed DOI PMC
Keating S.E., Blumer M., Grismer L.L., Lin A., Nielsen S.V., Thura M.K., Wood P.L., Jr., Quah E.S.H., Gamble T. Sex chromosome turnover in bent-toed geckos (Cyrtodactylus) Genes. 2021;12:116. doi: 10.3390/genes12010116. PubMed DOI PMC
Keating S.E., Greenbaum E., Johnson J.D., Gamble T. Identification of a cis-sex chromosome transition in banded geckos (Coleonyx, Eublepharidae, Gekkota) J. Evol. Biol. 2022;35:1675–1682. doi: 10.1111/jeb.14022. PubMed DOI
Pinto B.J., Keating S.E., Nielsen S.V., Scantlebury D.P., Daza J.D., Gamble T. Chromosome-level genome assembly reveals dynamic sex chromosomes in neotropical leaf-litter geckos (Sphaerodactylidae: Sphaerodactylus) J. Hered. 2022;113:272–287. doi: 10.1093/jhered/esac016. PubMed DOI PMC
Rovatsos M., Gamble T., Nielsen S.V., Georges A., Ezaz T., Kratochvíl L. Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos. Philos. Trans. R. Soc. B. 2021;376:20200102. doi: 10.1098/rstb.2020.0102. PubMed DOI PMC
Ratsoavina F.M., Raminosoa N.R., Louis E.E., Jr., Raselimanana A.P., Glaw F., Vences M. An overview of Madagascar’s leaf tailed geckos (genus Uroplatus): Species boundaries, candidate species and review of geographical distribution based on molecular data. Salamandra. 2013;49:115–148.
Solleder E., Schmid M. XX/XY-sex chromosomes in Gekko gecko (Sauria, Reptilia) Amphib.-Reptil. 1984;5:339–345. doi: 10.1163/156853884X-005-03-14. DOI
Tokunaga S. Temperature-dependent sex determination in Gekko japonicus (Gekkonidae, Reptilia) Dev. Growth Differ. 1985;27:117–120. doi: 10.1111/j.1440-169X.1985.00117.x. PubMed DOI
Yoshida M., Itoh M. Karyotype of the gecko, Gekko japonicus. Chrom. Info. Serv. 1974;17:29–31.
Kawai A., Ishijima J., Nishida C., Kosaka A., Ota H., Kohno S., Matsuda Y. The ZW sex chromosomes of Gekko hokouensis (Gekkonidae, Squamata) represent highly conserved homology with those of avian species. Chromosoma. 2009;118:43–51. doi: 10.1007/s00412-008-0176-2. PubMed DOI
Ding G.H., Yang J., Wang J., Ji X. Offspring sex in a TSD gecko correlates with an interaction between incubation temperature and yolk steroid hormones. Naturwissenschaften. 2012;99:999–1006. doi: 10.1007/s00114-012-0981-6. PubMed DOI
Koubová M., Johnson Pokorná M., Rovatsos M., Farkačová K., Altmanová M., Kratochvíl L. Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): Are differentiated sex chromosomes indeed so evolutionary stable? Chromosome Res. 2014;22:441–452. doi: 10.1007/s10577-014-9430-z. 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
Ota H., Hikida T., Matsui M., Mori A. Karyotypes of two species of the genus Cyrtodactylus (Squamata: Gekkonidae) from Sarawak, Malaysia. Caryologia. 1992;45:43–49. doi: 10.1080/00087114.1992.10797209. DOI
Ota H., Hikida T., Nabhitabhata J., Panha S. Cryptic taxonomic diversity in two broadly distributed lizards of Thailand (Mabuya macularia and Dixonius siamensis) as revealed by chromosomal investigations (Reptilia: Lacertilia) Nat. Hist. J. Chulalongkorn Univ. 2001;1:1–7.
Trifonov V.A., Giovannotti M., O’Brien P.C., Wallduck M., Lovell F., Rens W., Parise-Maltempi P.P., Caputo V., Ferguson-Smith M.A. Chromosomal evolution in Gekkonidae. I. Chromosome painting between Gekko and Hemidactylus species reveals phylogenetic relationships within the group. Chromosome Res. 2011;19:843–855. doi: 10.1007/s10577-011-9241-4. PubMed DOI
Mezzasalma M., Brunelli E., Odierna G., Guarino F.M. First insights on the karyotype diversification of the endemic malagasy leaf-toed geckos (Squamata: Gekkonidae: Uroplatus) Animals. 2022;12:2054. doi: 10.3390/ani12162054. PubMed DOI PMC
Mazzoleni S., Augstenová B., Clemente L., Auer M., Fritz U., Praschag P., Protiva T., Velenský P., Kratochvíl L., Rovatsos M. Turtles of the genera Geoemyda and Pangshura (Testudines: Geoemydidae) lack differentiated sex chromosomes: The end of a 40-year error cascade for Pangshura. PeerJ. 2019;7:e6241. doi: 10.7717/peerj.6241. PubMed DOI PMC
Sumner A.T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 1972;75:304–306. doi: 10.1016/0014-4827(72)90558-7. PubMed DOI
Ijdo J.W., Wells R.A., Baldini A., Reeders S.T. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 1991;19:4780. doi: 10.1093/nar/19.17.4780. PubMed DOI PMC
Rovatsos M., Johnson Pokorná M., Altmanová M., Kratochvíl L. Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): Differentiation of sex and neo-sex chromosomes. Sci. Rep. 2015;5:13196. doi: 10.1038/srep13196. PubMed DOI PMC
Endow S.A. Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics. 1982;100:375–385. doi: 10.1093/genetics/100.3.375. PubMed DOI PMC
Bolger A.M., Lohse M., Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Liu Y., Zhou Q., Wang Y., Luo L., Yang J., Yang L., Liu M., Li Y.R., Qian T.M., Zheng Y., et al. Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration. Nat. Commun. 2015;24:10033. doi: 10.1038/ncomms10033. PubMed DOI PMC
Rovatsos M., Kratochvíl L. Molecular sexing applicable in 4000 species of lizards and snakes? From dream to real possibility. Methods Ecol. Evol. 2017;8:902–906. doi: 10.1111/2041-210X.12714. DOI
Pyron R.A., Burbrink F.T. Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol. Lett. 2014;17:13–21. doi: 10.1111/ele.12168. PubMed DOI
Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012;13:134. doi: 10.1186/1471-2105-13-134. PubMed DOI PMC
Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B.C., Remm M., Rozen S.G. Primer3—New capabilities and interfaces. Nucleic Acids Res. 2012;40:e115. doi: 10.1093/nar/gks596. PubMed DOI PMC
Kratochvíl L., Gamble T., Rovatsos M. Sex chromosome evolution among amniotes: Is the origin of sex chromosomes non-random? Philos. Trans. R. Soc. B. 2021;376:20200108. doi: 10.1098/rstb.2020.0108. PubMed DOI PMC
Rovatsos M., Rehák I., Velenský P., Kratochvíl L. Shared ancient sex chromosomes in varanids, beaded lizards, and alligator lizards. Mol. Biol. Evol. 2019;36:1113–1120. doi: 10.1093/molbev/msz024. PubMed DOI
Pan Q., Kay T., Depincé A., Adolfi M., Schartl M., Guiguen Y., Herpin A. Evolution of master sex determiners: TGF-β signalling pathways at regulatory crossroads. Philos. Trans. R. Soc. B. 2021;376:20200091. doi: 10.1098/rstb.2020.0091. PubMed DOI PMC
Adolfi M.C., Herpin A., Schartl M. The replaceable master of sex determination: Bottom-up hypothesis revisited. Philos. Trans. R. Soc. B. 2021;376:20200090. doi: 10.1098/rstb.2020.0090. PubMed DOI PMC
Kurokawa H., Saito D., Nakamura S., Katoh-Fukui Y., Ohta K., Baba T., Morohashi K., Tanaka M. Germ cells are essential for sexual dimorphism in the medaka gonad. Proc. Natl. Acad. Sci. USA. 2007;104:16958–16963. doi: 10.1073/pnas.0609932104. PubMed DOI PMC
King M. Chromosomal and immunogenetic data: A new perspective on the origin of Australia’s reptiles. In: Olmo E., editor. Cytogenetics of Amphibians and Reptiles. Birkhäuser Verlag; Basel, Switzerland: 1990. pp. 153–180.
Gorman G.C. The chromosomes of the Reptilia, a cytotaxonomic interpretation. In: Chiarelli A.B., Capanna E., editors. Cytotaxonomy and Vertebrate Evolution. Academic Press; London, UK: 1973. pp. 349–424.
Johnson Pokorná M., Trifonov V.A., Rens W., Ferguson-Smith M.A., Kratochvíl L. Low rate of interchromosomal rearrangements during old radiation of gekkotan lizards (Squamata: Gekkota) Chromosome Res. 2015;23:299–309. doi: 10.1007/s10577-015-9468-6. PubMed DOI
Suwala G., Altmanová M., Mazzoleni S., Karameta E., Pafilis P., Kratochvíl L., Rovatsos M. Evolutionary variability of W-linked repetitive content in lacertid lizards. Genes. 2020;11:531. doi: 10.3390/genes11050531. PubMed DOI PMC
De Smet W.H. Description of the orcein stained karyotypes of 36 lizard species (Lacertilia, Reptilia) belonging to the families Teiidae, Scincidae, Lacertidae, Cordylidae and Varanidae (Autarchoglossa) Acta Zool. Pathol. Antverp. 1981;76:73–118.
Odierna G., Caprigilone T., Kupriyanova L.A., Olmo E. Further data on sex chromosomes of Lacertidae and a hypothesis on their evolutionary trend. Amphibia-Reptilia. 1993;14:1–11. doi: 10.1163/156853893X00147. DOI
Rovatsos M., Marchal J.A., Giagia-Athanasopoulou E., Sánchez A. Molecular composition of heterochromatin and its contribution to chromosome variation in the Microtus thomasi/Microtus atticus species complex. Genes. 2021;12:807. doi: 10.3390/genes12060807. PubMed DOI PMC
Acosta M.J., Marchal J.A., Fernández-Espartero C., Romero-Fernández I., Rovatsos M.T., Giagia-Athanasopoulou E.B., Gornung E., Castiglia R., Sánchez A. Characterization of the satellite DNA Msat-160 from species of Terricola (Microtus) and Arvicola (Rodentia, Arvicolinae) Genetica. 2010;138:1085–1098. doi: 10.1007/s10709-010-9496-2. PubMed DOI
Hughes J.F., Skaletsky H., Pyntikova T., Graves T.A., van Daalen S.K.M., Minx P.J., Fulton R.S., McGrath S.D., Locke D.P., Friedman C., et al. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature. 2010;463:536–539. doi: 10.1038/nature08700. PubMed DOI PMC
Rovatsos M.T., Marchal J.A., Romero-Fernández I., Giagia-Athanasopoulou E.B., Sánchez A. Molecular and physical characterization of the complex pericentromeric heterochromatin of the vole species Microtus thomasi. Cytogenet. Genome Res. 2014;144:131–141. doi: 10.1159/000368648. PubMed DOI
Shirleen Soh Y.Q., Alföldi J., Pyntikova T., Brown L.G., Graves T., Minx P.J., Fulton R.S., Kremitzki C., Koutseva N., Mueller J.L., et al. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell. 2014;159:800–813. doi: 10.1016/j.cell.2014.09.052. 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
Morgan A.P., Pardo-Manuel de Villena F. Sequence and structural diversity of mouse Y chromosomes. Mol. Biol. Evol. 2017;34:3186–3204. doi: 10.1093/molbev/msx250. PubMed DOI PMC
Augstenová B., Mazzoleni S., Kratochvíl L., Rovatsos M. Evolutionary dynamics of the W chromosome in caenophidian snakes. Genes. 2017;9:5. doi: 10.3390/genes9010005. PubMed DOI PMC
Rovatsos M., Altmanová M., Augstenová B., Mazzoleni S., Velenský P., Kratochvíl L. ZZ/ZW sex determination with multiple neo-sex chromosomes is common in Madagascan chameleons of the genus Furcifer (Reptilia: Chamaeleonidae) Genes. 2019;10:1020. doi: 10.3390/genes10121020. PubMed DOI PMC
Marshall Graves J.A. Sex chromosome specialization and degeneration in mammals. Cell. 2006;124:901–914. doi: 10.1016/j.cell.2006.02.024. PubMed DOI
Griffin D.K. Is the Y chromosome disappearing? Both sides of the argument. Chromosome Res. 2012;20:35–45. doi: 10.1007/s10577-011-9252-1. PubMed DOI
Bachtrog D., Mank J.E., Peichel C.L., Kirkpatrick M., Otto S.P., Ashman T.-L., Hahn M.W., Kitano J., Mayrose I., Ming R., et al. Sex determination: Why so many ways of doing it? PLoS Biol. 2014;12:e1001899. doi: 10.1371/journal.pbio.1001899. PubMed DOI PMC
Rovatsos M., Kratochvíl L. Evolution of dosage compensation does not depend on genomic background. Mol. Ecol. 2021;30:1836–1845. doi: 10.1111/mec.15853. PubMed DOI
Sex Chromosome Turnovers and Stability in Snakes
Cytogenetic Analysis of Satellitome of Madagascar Leaf-Tailed Geckos
Robertsonian fusion triggers recombination suppression on sex chromosomes in Coleonyx geckos
Cytogenetic Analysis of Seven Species of Gekkonid and Phyllodactylid Geckos