Heteromorphic ZZ/ZW sex chromosomes sharing gene content with mammalian XX/XY are conserved in Madagascan chameleons of the genus Furcifer.
Chameleons
Homology
Karyotypes
Microdissection
Sex chromosomes
qPCR
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 Feb 2024
28 Feb 2024
Historique:
received:
01
12
2023
accepted:
23
02
2024
medline:
29
2
2024
pubmed:
29
2
2024
entrez:
28
2
2024
Statut:
epublish
Résumé
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 Z
Identifiants
pubmed: 38418601
doi: 10.1038/s41598-024-55431-9
pii: 10.1038/s41598-024-55431-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4898Subventions
Organisme : Grantová Agentura České Republiky
ID : 23-07347S
Organisme : Charles University Research Centre Program
ID : 204069
Informations de copyright
© 2024. The Author(s).
Références
Johnson Pokorná, M. & Kratochvíl, L. What was the ancestral sex-determining mechanism in amniote vertebrates?. Biol. Rev. 91, 1–12. https://doi.org/10.1111/brv.12156 (2016).
doi: 10.1111/brv.12156
pubmed: 25424152
Pla, S., Maynou, F. & Piferrer, F. Hermaphroditism in fish: Incidence, distribution and associations with abiotic environmental factors. Rev. Fish Biol. Fish. 31, 935–955. https://doi.org/10.1007/S11160-021-09681-9 (2021).
doi: 10.1007/S11160-021-09681-9
Pla, S., Benvenuto, C., Capellini, I. & Piferrer, F. Switches, stability and reversals in the evolutionary history of sexual systems in fish. Nat. Commun. 13, 3029. https://doi.org/10.1038/s41467-022-30419-z (2022).
doi: 10.1038/s41467-022-30419-z
pubmed: 35637181
pmcid: 9151764
Jeffries, D. L., Gerchen, J. F., Scharmann, M. & Pannell, J. R. A neutral model for the loss of recombination on sex chromosomes. Philos. Trans. R. Soc. B Biol. Sci. 376, 20200096. https://doi.org/10.1098/rstb.2020.0096 (2021).
doi: 10.1098/rstb.2020.0096
pubmed: 34247504
pmcid: 8273504
Kratochvíl, L. et al. Expanding the classical paradigm: What we have learnt from vertebrates about sex chromosome evolution. Philos. Trans. R. Soc. B 376, 20200097. https://doi.org/10.1098/rstb.2020.0097 (2021).
doi: 10.1098/rstb.2020.0097
pubmed: 34304593
pmcid: 8310716
Abbott, J. K., Nordén, A. K. & Hansson, B. Sex chromosome evolution: Historical insights and future perspectives. Proc. R. Soc. B Biol. Sci. 284, 20162806. https://doi.org/10.1098/rspb.2016.2806 (2017).
doi: 10.1098/rspb.2016.2806
Furman, B. L. S. et al. Sex chromosome evolution: So many exceptions to the rules. Genome Biol. Evol. 12, 750–763. https://doi.org/10.1093/gbe/evaa081 (2020).
doi: 10.1093/gbe/evaa081
pubmed: 32315410
pmcid: 7268786
Kratochvíl, L., Gamble, T. & Rovatsos, M. Sex chromosome evolution among amniotes: Is the origin of sex chromosomes non-random?. Philos. Trans. R. Soc. B 376, 20200108. https://doi.org/10.1098/rstb.2020.0108 (2021).
doi: 10.1098/rstb.2020.0108
pubmed: 34304592
pmcid: 8310715
Marshall Graves, J. A. & Peichel, C. L. Are homologies in vertebrate sex determination due to shared ancestry or to limited options?. Genome Biol. 11, 205. https://doi.org/10.1186/gb-2010-11-4-205 (2010).
doi: 10.1186/gb-2010-11-4-205
pubmed: 20441602
pmcid: 2884537
Kostmann, A., Kratochvíl, L. & Rovatsos, M. Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proc. R. Soc. B Biol. Sci. 288, 20202139. https://doi.org/10.1098/rspb.2020.2139 (2021).
doi: 10.1098/rspb.2020.2139
Saunders, P. A. & Veyrunes, F. Unusual mammalian sex determination systems: A cabinet of curiosities. Genes 12, 1770. https://doi.org/10.3390/genes12111770 (2021).
doi: 10.3390/genes12111770
pubmed: 34828376
pmcid: 8617835
Nielsen, S. V. et al. Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata). Biol. Lett. 15, 20190498. https://doi.org/10.1098/rsbl.2019.0498 (2019).
doi: 10.1098/rsbl.2019.0498
pubmed: 31594492
pmcid: 6832183
Gamble, T. et al. Restriction site-Associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 32, 1296–1309. https://doi.org/10.1093/molbev/msv023 (2015).
doi: 10.1093/molbev/msv023
pubmed: 25657328
Rovatsos, M., Praschag, P., Fritz, U. & Kratochvíl, L. Stable Cretaceous sex chromosomes enable molecular sexing in softshell turtles (Testudines: Trionychidae). Sci. Rep. 7, 42150. https://doi.org/10.1038/srep42150 (2017).
doi: 10.1038/srep42150
pubmed: 28186115
pmcid: 5301483
Rovatsos, M., Rehák, I., Velenský, P. & Kratochvíl, L. Shared ancient sex chromosomes in varanids, beaded lizards, and alligator lizards. Mol. Biol. Evol. 36, 1113–1120. https://doi.org/10.1093/molbev/msz024 (2019).
doi: 10.1093/molbev/msz024
pubmed: 30722046
Rovatsos, M. et al. 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. 376, 20200102. https://doi.org/10.1098/rstb.2020.0102 (2021).
doi: 10.1098/rstb.2020.0102
pubmed: 34304587
pmcid: 8310713
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. 13, evab119. https://doi.org/10.1093/gbe/evab119 (2021).
doi: 10.1093/gbe/evab119
pubmed: 34051083
pmcid: 8290109
Ezaz, T. et al. Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Res. 17, 91–98. https://doi.org/10.1007/s10577-008-9019-5 (2009).
doi: 10.1007/s10577-008-9019-5
pubmed: 19172405
Whiteley, S. L., Georges, A., Weisbecker, V., Schwanz, L. E. & Holleley, C. E. Ovotestes suggest cryptic genetic influence in a reptile model for temperature-dependent sex determination. Proc. R. Soc. B Biol. Sci. 288, 20202819. https://doi.org/10.1098/rspb.2020.2819 (2021).
doi: 10.1098/rspb.2020.2819
Uetz, P., Freed, P., Aguilar, R., Reyes, F., & Hošek, J. (eds.) The Reptile Database. http://www.reptile-database.org . Accessed 30 Jan 2022.
Nielsen, S. V., Banks, J. L., Diaz, R. E., Trainor, P. A. & Gamble, T. Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae). J. Evol. Biol. 31, 484–490. https://doi.org/10.1111/jeb.13242 (2018).
doi: 10.1111/jeb.13242
pubmed: 29345015
Sidhom, M. et al. Karyological characterization of the common chameleon (Chamaeleo chamaeleon) provides insights on the evolution and diversification of sex chromosomes in Chamaeleonidae. Zoology 141, 125738. https://doi.org/10.1016/j.zool.2019.125738 (2020).
doi: 10.1016/j.zool.2019.125738
pubmed: 32291142
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. 5, 13196. https://doi.org/10.1038/srep13196 (2015).
doi: 10.1038/srep13196
pubmed: 26286647
pmcid: 4541320
Rovatsos, M. et al. ZZ/ZW sex determination with multiple neo-sex chromosomes is common in Madagascan chameleons of the genus Furcifer (Reptilia: Chamaeleonidae). Genes 10, 1020. https://doi.org/10.3390/genes10121020 (2019).
doi: 10.3390/genes10121020
pubmed: 31817782
pmcid: 6947276
Pokorná, M., Altmanová, M. & Kratochvíl, L. Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 22, 35–44. https://doi.org/10.1007/s10577-014-9403-2 (2014).
doi: 10.1007/s10577-014-9403-2
pubmed: 24590843
Pennell, M. W. et al. Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet. 11, e1005237. https://doi.org/10.1371/journal.pgen.1005237 (2015).
doi: 10.1371/journal.pgen.1005237
pubmed: 25993542
pmcid: 4439076
Sember, A. et al. 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. 376, 20200098. https://doi.org/10.1098/rstb.2020.0098 (2021).
doi: 10.1098/rstb.2020.0098
pubmed: 34304595
pmcid: 8310710
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, e6241. https://doi.org/10.7717/peerj.6241/supp-1 (2019).
doi: 10.7717/peerj.6241/supp-1
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 12, 779. https://doi.org/10.3390/genes12050779 (2021).
doi: 10.3390/genes12050779
pubmed: 34065205
pmcid: 8160951
Zhu, Z. X. et al. Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing. Zool. Res. 43, 719–733. https://doi.org/10.24272/j.issn.2095-8137.2022.127 (2022).
doi: 10.24272/j.issn.2095-8137.2022.127
pubmed: 35927394
pmcid: 9486513
Marchal, J. A. et al. X chromosome painting in Microtus: Origin and evolution of the giant sex chromosomes. Chromosome Res. 12, 767–776. https://doi.org/10.1007/s10577-005-5077-0 (2004).
doi: 10.1007/s10577-005-5077-0
pubmed: 15702415
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).
doi: 10.1093/bioinformatics/btu170
pubmed: 24695404
pmcid: 4103590
Alföldi, J. et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587–591. https://doi.org/10.1038/nature10390 (2011).
doi: 10.1038/nature10390
pubmed: 21881562
pmcid: 3184186
Cornejo-Páramo, P. et al. Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes. Genome Biol. Evol. 12, 924–930. https://doi.org/10.1093/gbe/evaa104 (2020).
doi: 10.1093/gbe/evaa104
pubmed: 32433751
pmcid: 7313667
Vicoso, B., Emerson, J. J., Zektser, Y., Mahajan, S. & Bachtrog, D. Comparative sex chromosome genomics in snakes: Differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11, e1001643. https://doi.org/10.1371/journal.pbio.1001643 (2013).
doi: 10.1371/journal.pbio.1001643
pubmed: 24015111
pmcid: 3754893
Rovatsos, M. & Kratochvíl, L. Evolution of dosage compensation does not depend on genomic background. Mol. Ecol. 30, 1836–1845. https://doi.org/10.1111/MEC.15853 (2021).
doi: 10.1111/MEC.15853
pubmed: 33606326
Pensabene, E., Yurchenko, A., Kratochvíl, L. & Rovatsos, M. Madagascar leaf-tail geckos (Uroplatus spp.) share independently evolved differentiated ZZ/ZW sex chromosomes. Cells 12, 260. https://doi.org/10.3390/cells12020260 (2023).
doi: 10.3390/cells12020260
pubmed: 36672195
pmcid: 9856856
Nguyen, P. et al. Neo-sex chromosomes and adaptive potential in tortricid pests. Proc. Natl. Acad. Sci. USA 110, 6931–6936. https://doi.org/10.1073/pnas.1220372110 (2013).
doi: 10.1073/pnas.1220372110
pubmed: 23569222
pmcid: 3637691
Rovatsos, M., Altmanová, M., Pokorná, M. & Kratochvíl, L. Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution 68, 2079–2085. https://doi.org/10.1111/evo.12357 (2014).
doi: 10.1111/evo.12357
pubmed: 24433436
Rovatsos, M., Farkačová, K., Altmanová, M., Johnson Pokorná, M. & Kratochvíl, L. The rise and fall of differentiated sex chromosomes in geckos. Mol. Ecol. 28, 3042–3052. https://doi.org/10.1111/mec.15126 (2019).
doi: 10.1111/mec.15126
pubmed: 31063656
Rovatsos, M., Pokorná, M., Altmanová, M. & Kratochvíl, L. Cretaceous park of sex determination: Sex chromosomes are conserved across iguanas. Biol. Lett. 10, 20131093–20131093. https://doi.org/10.1098/rsbl.2013.1093 (2014).
doi: 10.1098/rsbl.2013.1093
pubmed: 24598109
pmcid: 3982436
Altmanová, M. et al. All iguana families with the exception of basilisks share sex chromosomes. Zoology 126, 98–102. https://doi.org/10.1016/j.zool.2017.11.007 (2017).
doi: 10.1016/j.zool.2017.11.007
pubmed: 29287619
Ye, J. et al. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 13, 134. https://doi.org/10.1186/1471-2105-13-134 (2012).
doi: 10.1186/1471-2105-13-134
Untergasser, A. et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 40, e115. https://doi.org/10.1093/nar/gks596 (2012).
doi: 10.1093/nar/gks596
pubmed: 22730293
pmcid: 3424584
Tonini, J. F. R., Beard, K. H., Ferreira, R. B., Jetz, W. & Pyron, A. R. Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv. 204, 23–31. https://doi.org/10.1016/j.biocon.2016.03.039 (2016).
doi: 10.1016/j.biocon.2016.03.039
Mezzasalma, M. et al. Microchromosome fusions underpin convergent evolution of chameleon karyotypes. Evolution 77, 1930–1944. https://doi.org/10.1093/evolut/qpad097 (2023).
doi: 10.1093/evolut/qpad097
pubmed: 37288542
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. 13, 93. https://doi.org/10.1186/1471-2148-13-93 (2013).
doi: 10.1186/1471-2148-13-93
pubmed: 23627680
pmcid: 3682911
Tolley, K. A., Townsend, T. M. & Vences, M. Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proc. R. Soc. B Biol. Sci. 280, 20130184. https://doi.org/10.1098/rspb.2013.0184 (2013).
doi: 10.1098/rspb.2013.0184
Zheng, Y. & Wiens, J. J. 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. 94, 537–547. https://doi.org/10.1016/j.ympev.2015.10.009 (2016).
doi: 10.1016/j.ympev.2015.10.009
pubmed: 26475614
Pyron, R. A. Novel approaches for phylogenetic inference from morphological data and total-evidence dating in squamate reptiles (lizards, snakes, and amphisbaenians). Syst. Biol. 66, 38–56. https://doi.org/10.1093/sysbio/syw068 (2017).
doi: 10.1093/sysbio/syw068
pubmed: 28173602
Rovatsos, M., Vukić, J., Lymberakis, P. & Kratochvíl, L. Evolutionary stability of sex chromosomes in snakes. Proc. R. Soc. B Biol. Sci. 282, 20151992. https://doi.org/10.1098/rspb.2015.1992 (2015).
doi: 10.1098/rspb.2015.1992
Xie, H., Chen, Z., Pang, S. & Du, W. Efficient and highly continuous chromosome-level genome assembly of the first chameleon genome. Genome Biol. Evol. 15, evad131. https://doi.org/10.1093/gbe/evad131 (2023).
doi: 10.1093/gbe/evad131
pubmed: 37481259
pmcid: 10410292
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
doi: 10.1016/S0022-2836(05)80360-2
pubmed: 2231712
Charlesworth, D. The timing of genetic degeneration of sex chromosomes. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 376, 20200093. https://doi.org/10.1098/rstb.2020.0093 (2021).
doi: 10.1098/rstb.2020.0093
pubmed: 34247501
pmcid: 8273506
Fontaine, A. et al. Extensive genetic differentiation between homomorphic sex chromosomes in the mosquito vector, Aedes aegypti. Genome Biol. Evol. 9, 2322–2335. https://doi.org/10.1093/gbe/evx171 (2017).
doi: 10.1093/gbe/evx171
pubmed: 28945882
pmcid: 5737474
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. 12, 90. https://doi.org/10.1186/1471-2156-12-90 (2011).
doi: 10.1186/1471-2156-12-90
pubmed: 22013909
pmcid: 3215666
Rovatsos, M., Vukić, J. & Kratochvíl, L. Mammalian X homolog acts as sex chromosome in lacertid lizards. Heredity 117, 8–13. https://doi.org/10.1038/hdy.2016.18 (2016).
doi: 10.1038/hdy.2016.18
pubmed: 26980341
pmcid: 4901352
Pensabene, E., Kratochvíl, L. & Rovatsos, M. Independent evolution of sex chromosomes in eublepharid geckos, a lineage with environmental and genotypic sex determination. Life 10, 342. https://doi.org/10.3390/life10120342 (2020).
doi: 10.3390/life10120342
pubmed: 33322017
pmcid: 7763811
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 119, 2116475119. https://doi.org/10.1073/pnas.2116475119 (2022).
doi: 10.1073/pnas.2116475119
Rovatsos, M. et al. Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards. Sci. Rep. 9, 7832. https://doi.org/10.1038/s41598-019-44192-5 (2019).
doi: 10.1038/s41598-019-44192-5
pubmed: 31127134
pmcid: 6534595
Petraccioli, A. et al. Isolation and characterization of interspersed repeated sequences in the common lizard, Zootoca vivipara, and their conservation in Squamata. Cytogenet. Genome Res. 157, 65–76. https://doi.org/10.1159/000497304 (2019).
doi: 10.1159/000497304
pubmed: 30836364
Ahmad, S. F., 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 8, 27. https://doi.org/10.3390/genes11070827 (2020).
doi: 10.3390/genes11070827
Takehana, Y. et al. Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat. Commun. 5, 4157. https://doi.org/10.1038/ncomms5157 (2014).
doi: 10.1038/ncomms5157
pubmed: 24948391
Fujii, J. et al. Involvement of androgen receptor in sex determination in an amphibian species. PLoS One 9, e93655. https://doi.org/10.1371/journal.pone.0093655 (2014).
doi: 10.1371/journal.pone.0093655
pubmed: 24826887
pmcid: 4020753