Heteromorphic ZZ/ZW sex chromosomes sharing gene content with mammalian XX/XY are conserved in Madagascan chameleons of the genus Furcifer
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
23-07347S
Grantová Agentura České Republiky
204069
Charles University Research Centre Program
PubMed
38418601
PubMed Central
PMC10901801
DOI
10.1038/s41598-024-55431-9
PII: 10.1038/s41598-024-55431-9
Knihovny.cz E-zdroje
- Klíčová slova
- Chameleons, Homology, Karyotypes, Microdissection, Sex chromosomes, qPCR,
- MeSH
- ještěři * genetika MeSH
- molekulární evoluce MeSH
- pohlavní chromozomy genetika MeSH
- procesy určující pohlaví genetika MeSH
- savci genetika MeSH
- sekvence nukleotidů MeSH
- variabilita počtu kopií segmentů DNA * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Chameleons are well-known lizards with unique morphology and physiology, but their sex determination has remained poorly studied. Madagascan chameleons of the genus Furcifer have cytogenetically distinct Z and W sex chromosomes and occasionally Z1Z1Z2Z2/Z1Z2W multiple neo-sex chromosomes. To identify the gene content of their sex chromosomes, we microdissected and sequenced the sex chromosomes of F. oustaleti (ZZ/ZW) and F. pardalis (Z1Z1Z2Z2/Z1Z2W). In addition, we sequenced the genomes of a male and a female of F. lateralis (ZZ/ZW) and F. pardalis and performed a comparative coverage analysis between the sexes. Despite the notable heteromorphy and distinctiveness in heterochromatin content, the Z and W sex chromosomes share approximately 90% of their gene content. This finding demonstrates poor correlation of the degree of differentiation of sex chromosomes at the cytogenetic and gene level. The test of homology based on the comparison of gene copy number variation revealed that female heterogamety with differentiated sex chromosomes remained stable in the genus Furcifer for at least 20 million years. These chameleons co-opted for the role of sex chromosomes the same genomic region as viviparous mammals, lacertids and geckos of the genus Paroedura, which makes these groups excellent model for studies of convergent and divergent evolution of sex chromosomes.
Department of Ecology Faculty of Science Charles University Prague Czech Republic
Department of Experimental Biology University of Jaén Jaén Spain
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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
Pla S, Maynou F, Piferrer F. Hermaphroditism in fish: Incidence, distribution and associations with abiotic environmental factors. Rev. Fish Biol. Fish. 2021;31:935–955. doi: 10.1007/S11160-021-09681-9. DOI
Pla S, Benvenuto C, Capellini I, Piferrer F. Switches, stability and reversals in the evolutionary history of sexual systems in fish. Nat. Commun. 2022;13:3029. doi: 10.1038/s41467-022-30419-z. PubMed DOI PMC
Jeffries DL, Gerchen JF, Scharmann M, Pannell JR. A neutral model for the loss of recombination on sex chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. . 2021;376:20200096. doi: 10.1098/rstb.2020.0096. PubMed DOI PMC
Kratochvíl L, et al. Expanding the classical paradigm: What we have learnt from vertebrates about sex chromosome evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. . 2021;376:20200097. doi: 10.1098/rstb.2020.0097. PubMed DOI PMC
Abbott JK, Nordén AK, Hansson B. Sex chromosome evolution: Historical insights and future perspectives. Proc. R. Soc. B Biol. Sci. 2017;284:20162806. doi: 10.1098/rspb.2016.2806. PubMed DOI PMC
Furman BLS, Metzger DCH, Darolti I, Wright AE, Sandkam BA, Almeida P, Shu JJ, Mank JE, Fraser B. Sex chromosome evolution: So many exceptions to the rules. Genome Biol. Evol. 2020;12:750–763. doi: 10.1093/gbe/evaa081. 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. Lond. B Biol. Sci. . 2021;376:20200108. doi: 10.1098/rstb.2020.0108. PubMed DOI PMC
Marshall Graves JA, Peichel CL. Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol. 2010;11:205. doi: 10.1186/gb-2010-11-4-205. 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 Biol. Sci. 2021;288:20202139. doi: 10.1098/rspb.2020.2139. PubMed DOI PMC
Saunders PA, Veyrunes F. Unusual mammalian sex determination systems: A cabinet of curiosities. Genes. 2021;12:1770. doi: 10.3390/genes12111770. PubMed DOI PMC
Nielsen SV, Guzmán-Méndez IA, Gamble T, Blumer M, Pinto BJ, Kratochvíl L, Rovatsos M. Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata) Biol. Lett. 2019;15:20190498. doi: 10.1098/rsbl.2019.0498. PubMed DOI PMC
Gamble T, Coryell J, Ezaz T, Lynch J, Scantlebury DP, 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
Rovatsos M, Praschag P, Fritz U, Kratochvíl L. Stable Cretaceous sex chromosomes enable molecular sexing in softshell turtles (Testudines: Trionychidae) Sci. Rep. 2017;7:42150. doi: 10.1038/srep42150. 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
Rovatsos M, Gamble T, Nielsen SV, 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. Lond. B Biol. Sci. . 2021;376:20200102. doi: 10.1098/rstb.2020.0102. 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
Ezaz T, Quinn AE, Sarre SD, O’Meally D, Georges A, Marshall Graves JA. Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Res. 2009;17:91–98. doi: 10.1007/s10577-008-9019-5. PubMed DOI
Whiteley SL, Georges A, Weisbecker V, Schwanz LE, Holleley CE. Ovotestes suggest cryptic genetic influence in a reptile model for temperature-dependent sex determination. Proc. R. Soc. B Biol. Sci. 2021;288:20202819. doi: 10.1098/rspb.2020.2819. PubMed DOI PMC
Uetz, P., Freed, P., Aguilar, R., Reyes, F., & Hošek, J. (eds.) The Reptile Database. http://www.reptile-database.org. Accessed 30 Jan 2022.
Nielsen SV, Banks JL, Diaz RE, Trainor PA, Gamble T. Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae) J. Evol. Biol. 2018;31:484–490. doi: 10.1111/jeb.13242. PubMed DOI
Sidhom M, Said K, Chatti N, Guarino FM, Odierna G, Petraccioli A, Picariello O, Mezzasalma M. Karyological characterization of the common chameleon ( Chamaeleo chamaeleon ) provides insights on the evolution and diversification of sex chromosomes in Chamaeleonidae. Zoology. 2020;141:125738. doi: 10.1016/j.zool.2019.125738. PubMed DOI
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
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
Pokorná M, Altmanová M, Kratochvíl L. Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 2014;22:35–44. doi: 10.1007/s10577-014-9403-2. PubMed DOI
Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL, Valenzuela N, Kitano J. Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet. 2015;11:e1005237. doi: 10.1371/journal.pgen.1005237. PubMed DOI PMC
Sember A, Nguyen P, Perez MF, Altmanová M, Ráb P, Cioffi MDB. Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: State of the art and future challenges. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2021;376:20200098. doi: 10.1098/rstb.2020.0098. PubMed DOI PMC
Mazzoleni S, et al. 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;2019:e6241. doi: 10.7717/peerj.6241/supp-1. PubMed DOI PMC
Lisachov A, et al. Amplified fragments of an autosome-borne gene constitute a significant component of the w sex chromosome of Eremias velox (Reptilia, Lacertidae) Genes. 2021;12:779. doi: 10.3390/genes12050779. PubMed DOI PMC
Zhu ZX, et al. Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing. Zool. Res. 2022;43:719–733. doi: 10.24272/j.issn.2095-8137.2022.127. PubMed DOI PMC
Marchal JA, Acosta MJ, Nietzel H, Sperling K, Bullejos M, Díaz De La Guardia R, Sánchez A. X chromosome painting in Microtus: Origin and evolution of the giant sex chromosomes. Chromosome Res. 2004;12:767–776. doi: 10.1007/s10577-005-5077-0. PubMed DOI
Bolger AM, 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
Alföldi J, et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477:587–591. doi: 10.1038/nature10390. PubMed DOI PMC
Cornejo-Páramo P, et al. Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes. Genome Biol. Evol. 2020;12:924–930. doi: 10.1093/gbe/evaa104. PubMed DOI PMC
Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D. Comparative sex chromosome genomics in snakes: Differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 2013;11:e1001643. doi: 10.1371/journal.pbio.1001643. 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
Pensabene E, Yurchenko A, Kratochvíl L, Rovatsos M. Madagascar leaf-tail geckos (Uroplatus spp.) share independently evolved differentiated ZZ/ZW sex chromosomes. Cells. 2023;12:260. doi: 10.3390/cells12020260. PubMed DOI PMC
Nguyen P, Sýkorová M, Šíchová J, Kůta V, Dalíková M, Čapková Frydrychová R, Neven LG, 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
Rovatsos M, Altmanová M, Pokorná M, Kratochvíl L. Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution. 2014;68:2079–2085. doi: 10.1111/evo.12357. 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
Rovatsos M, Pokorná M, Altmanová M, Kratochvíl L. Cretaceous park of sex determination: Sex chromosomes are conserved across iguanas. Biol. Lett. 2014;10:20131093–20131093. doi: 10.1098/rsbl.2013.1093. PubMed DOI PMC
Altmanová M, Rovatsos M, Johnson Pokorná M, Veselý M, Wagner F, Kratochvíl L. All iguana families with the exception of basilisks share sex chromosomes. Zoology. 2017;126:98–102. doi: 10.1016/j.zool.2017.11.007. PubMed DOI
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. 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 BC, Remm M, Rozen SG. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115. doi: 10.1093/nar/gks596. PubMed DOI PMC
Tonini JFR, Beard KH, Ferreira RB, Jetz W, Pyron AR. Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv. 2016;204:23–31. doi: 10.1016/j.biocon.2016.03.039. DOI
Mezzasalma M, Streicher JW, Guarino FM, Jones MEH, Loader SP, Odierna G, Cooper N. Microchromosome fusions underpin convergent evolution of chameleon karyotypes. Evolution. 2023;77:1930–1944. doi: 10.1093/evolut/qpad097. PubMed DOI
Pyron RA, Burbrink FT, Wiens JJ. 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
Tolley KA, Townsend TM, Vences M. Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proc. R. Soc. B Biol. Sci. 2013;280:20130184. doi: 10.1098/rspb.2013.0184. PubMed DOI PMC
Zheng Y, Wiens JJ. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 2016;94:537–547. doi: 10.1016/j.ympev.2015.10.009. PubMed DOI
Pyron RA. Novel approaches for phylogenetic inference from morphological data and total-evidence dating in squamate reptiles (lizards, snakes, and amphisbaenians) Syst. Biol. 2017;66:38–56. doi: 10.1093/sysbio/syw068. PubMed DOI
Rovatsos M, Vukić J, Lymberakis P, Kratochvíl L. Evolutionary stability of sex chromosomes in snakes. Proc. R. Soc. B Biol. Sci. 2015;282:20151992. doi: 10.1098/rspb.2015.1992. PubMed DOI PMC
Xie H, Chen Z, Pang S, Du W. Efficient and highly continuous chromosome-level genome assembly of the first chameleon genome. Genome Biol. Evol. 2023;15:evad131. doi: 10.1093/gbe/evad131. PubMed DOI PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Charlesworth D. The timing of genetic degeneration of sex chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. . 2021;376:20200093. doi: 10.1098/rstb.2020.0093. PubMed DOI PMC
Fontaine A, Filipović I, Fansiri T, Hoffmann AA, Cheng C, Kirkpatrick M, Rašić G, Lambrechts L. Extensive genetic differentiation between homomorphic sex chromosomes in the mosquito vector, Aedes aegypti. Genome Biol. Evol. 2017;9:2322–2335. doi: 10.1093/gbe/evx171. PubMed DOI PMC
Pokorná M, Kratochvíl L, Kejnovský E. Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox) BMC Genet. 2011;12:90. doi: 10.1186/1471-2156-12-90. PubMed DOI PMC
Rovatsos M, Vukić J, Kratochvíl L. Mammalian X homolog acts as sex chromosome in lacertid lizards. Heredity. 2016;117:8–13. doi: 10.1038/hdy.2016.18. PubMed DOI PMC
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
Zhang X, et al. Sex-specific splicing of Z- and W-borne nr5a1 alleles suggests sex determination is controlled by chromosome conformation. Proc. Natl. Acad. Sci. USA. 2022;119:2116475119. doi: 10.1073/pnas.2116475119. 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
Petraccioli A, Guarino FM, Kupriyanova L, Mezzasalma M, Odierna G, Picariello O, Capriglione T. Isolation and characterization of interspersed repeated sequences in the common lizard, Zootoca vivipara, and their conservation in Squamata. Cytogenet. Genome Res. 2019;157:65–76. doi: 10.1159/000497304. PubMed DOI
Ahmad SF, Singchat W, Jehangir M, Panthum T, Srikulnath K. Consequence of paradigm shift with repeat landscapes in reptiles: Powerful facilitators of chromosomal rearrangements for diversity and evolution. Genes. 2020;8:27. doi: 10.3390/genes11070827. PubMed DOI PMC
Takehana Y, et al. Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat. Commun. 2014;5:4157. doi: 10.1038/ncomms5157. PubMed DOI
Fujii J, Kodama M, Oike A, Matsuo Y, Min MS, Hasebe T, Ishizuya-Oka A, Kawakami K, Nakamura M. Involvement of androgen receptor in sex determination in an amphibian species. PLoS One. 2014;9:e93655. doi: 10.1371/journal.pone.0093655. PubMed DOI PMC