Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): differentiation of sex and neo-sex chromosomes

. 2015 Aug 19 ; 5 () : 13196. [epub] 20150819

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26286647

Amniotes possess variability in sex determining mechanisms, however, this diversity is still only partially known throughout the clade and sex determining systems still remain unknown even in such a popular and distinctive lineage as chameleons (Squamata: Acrodonta: Chamaeleonidae). Here, we present evidence for female heterogamety in this group. The Malagasy giant chameleon (Furcifer oustaleti) (chromosome number 2n = 22) possesses heteromorphic Z and W sex chromosomes with heterochromatic W. The panther chameleon (Furcifer pardalis) (2n = 22 in males, 21 in females), the second most popular chameleon species in the world pet trade, exhibits a rather rare Z1Z1Z2Z2/Z1Z2W system of multiple sex chromosomes, which most likely evolved from W-autosome fusion. Notably, its neo-W chromosome is partially heterochromatic and its female-specific genetic content has expanded into the previously autosomal region. Showing clear evidence for genotypic sex determination in the panther chameleon, we resolve the long-standing question of whether or not environmental sex determination exists in this species. Together with recent findings in other reptile lineages, our work demonstrates that female heterogamety is widespread among amniotes, adding another important piece to the mosaic of knowledge on sex determination in amniotes needed to understand the evolution of this important trait.

Zobrazit více v PubMed

Uetz P. & Hošek J. (eds). The reptile database. (2014) Available at: http://www.reptile-database.org (Accessed: 23th January 2015).

Tolley K. A., Townsend T. M. & Vences M. Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proc. R. Soc. B. 280, 20130184 (2013). PubMed PMC

Pokorná M. & Kratochvíl L. Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 156, 168–183 (2009).

Johnson Pokorná M. & Kratochvíl L. What was the ancestral sex-determining mechanism in amniote vertebrates? Biol. Rev. (2014). In press. 10.1111/brv.12156. PubMed DOI

Ezaz T. et al. Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Res. 17, 91–98 (2009). PubMed

Harlow P. S. in Temperature-Dependent Sex Determination in Vertebrates (eds. Valenzuela N. & Lance V. ), 42–52 (Smithsonian Institution Scholarly Press: Washington, DC, 2004).

Gamble T., Geneva A. J., Glor R. E. & Zarkower D. Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68, 1027–1041 (2014). PubMed PMC

Rovatsos M., Altmanová M., Pokorná M. & Kratochvíl L. Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution 68, 2079–2085 (2014). PubMed

Rovatsos M., Pokorná M., Altmanová M. & Kratochvíl L. Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol. Lett. 10, 20131093 (2014). PubMed PMC

Viets B. E., Ewert M. A., Talent L. G. & Nelson C. E. Sex-determining mechanisms in squamate reptiles. J. Exp. Zool. 270, 45–56 (1994).

Andrews R. M. Incubation temperature and sex ratio of the veiled chameleon (Chamaeleo calyptratus). J. Herpetol. 39, 515–518 (2005).

Olmo E. & Signorino G. Chromorep: A reptile chromosomes database. Chamaeleonidae. (2005) Available at: http://ginux.univpm.it/scienze/chromorep/3.2.1.1.2%20Chamaeleonidae.html (Accessed: 23th January 2015).

Bourgat R. M. Biogeographical interest of Chamaeleo pardalis Cuvier, 1829 (Reptilia, Squamata, Chamaeleonidae) on Reunion Island. Herpetologica 28, 22–24 (1972).

Cheke A. & Hume J. Lost Land of the Dodo. (T & A D Poyser: London, 2008).

Cole N. A Field Guide to the Reptiles and Amphibians of Mauritius. (Mauritian Wildlife Foundation: Vacoas, Mauritius, 2009).

Grbic D. et al. Phylogeography and support vector machine classification of colour variation in panther chameleons. Molecular Ecology, in press, 10.1111/mec.13241 (2015). PubMed DOI PMC

Jenkins R. K. B. et al. Furcifer pardalis. The IUCN Red List of Threatened Species. (2011) Available at: http://www.iucnredlist.org/details/172955/0 (Accessed 23th January 2015).

Jenkins R. K. B. et al. Furcifer oustaleti. The IUCN Red List of Threatened Species. (2011) Available at: http://www.iucnredlist.org/details/172866/0 (Accessed 23th January 2015).

Bourgat R. M. Caryotypes des caméléons malgaches et systématique: Synthèse des données acquises. Annales de l´Université de Madagascar, Série Sciences de la Nature et Mathématiques 9, 77–85 (1972).

Matthey R. & van Brink J. M. Note préliminaire sur la cytologie chromosomique comparée des Caméléons. Rev. Suisse Zool. 63, 241–246 (1956).

Matthey R. Cytologie comparée et taxonomie des Chamaeleontidae (Reptilia – Lacertilia). Rev. Suisse Zool. 64, 709–732 (1957).

Tolley K. A. & Herrel A. The Biology of Chameleons. (University of California Press: California, Berkeley and Los Angeles, 2013).

Nagy Z. T., Sonet G., Glaw F. & Vences M. First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. PLoS One 7, e34506 (2012). PubMed PMC

Johnson Pokorná M., Rovatsos M. & Kratochvíl L. Sex chromosomes and karyotype of the (nearly) mythical creature, the Gila monster, Heloderma suspectum (Squamata: Helodermatidae). PLoS One 9, e104716 (2014). PubMed PMC

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. (2015). In press. 10.1093/molbev/msv023. 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. 142, 190–196 (2014). PubMed

Odierna G., Olmo E. & Cobror O. C-band variability in some Lacertidae (Sauria, Reptilia). Experientia 41, 944–946 (1985).

Koubová M. et al. Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): are differentiated sex chromosomes indeed so evolutionary stable? Chromosome Res. 22, 441–452 (2014). PubMed

Oguiura N., Ferrarezzi H. & Batistic R. F. Cytogenetics and molecular data in snakes: A phylogenetic approach. Cytogenet. Genome Res. 127, 128–142 (2009). PubMed

Mezzasalma M. et al. Chromosome evolution in pseudoxyrhophiine snakes from Madagascar: a wide range of karyotypic variability. Biol. J. Linn. Soc. 112, 450–460 (2014).

Ezaz T., Sarre S. D., O’Meally D., Graves J. & Georges A. Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet. Genome Res. 127, 249–260 (2009). PubMed

Young M. J., O’Meally D., Sarre S. D., Georges A. & Ezaz T. Molecular cytogenetic map of the central bearded dragon, Pogona vitticeps (Squamata: Agamidae). Chromosome Res. 21, 361–374 (2013). PubMed

Schmid M., Steinlein C., Haaf T. & Mijares-Urrutia A. Nascent ZW sex chromosomes in Thecadactylus rapicauda (Reptilia, Squamata, Phyllodactylidae). Cytogenet. Genome Res. 143, 259–267 (2014). PubMed

Rovatsos M. T. et al. Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res. 19, 869–882 (2011). PubMed

Rovatsos M. T. et al. Molecular and physical characterization of the complex pericentromeric heterochromatin of the vole species Microtus thomasi. Cytogenet. Genome Res. 144, 131–141 (2014). PubMed

Bachtrog D., Hom E., Wong K. M., Maside X. & de Jong P. Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol. 9, R30 (2008). PubMed PMC

Zhou Q. & Bachtrog D. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337, 341–345 (2012). PubMed PMC

Pokorná M., Altmanová M. & Kratochvíl L. Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 22, 35–44 (2014). PubMed

Srikulnath K. et al. Karyological characterization of the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Squamata) by molecular cytogenetic approach. Cytogenet. Genome Res. 125, 213–23 (2009). PubMed

Srikulnath K. et al. Chromosomal localization of the 18S-28S and 5S rRNA genes and (TTAGGG)n sequences of butterfly lizards (Leiolepis belliana belliana and Leiolepis boehmei, Agamidae, Squamata). Genet. Mol. Biol. 586, 582–586 (2011). PubMed PMC

Rojo V. et al. Karyological characterization of the endemic Iberian rock lizard, Iberolacerta monticola (Squamata, Lacertidae): insights into sex chromosome evolution. Cytogenet. Genome Res. 142, 28–39 (2014). PubMed

Srikulnath K., Uno Y., Nishida C. & Matsuda Y. Karyotype evolution in monitor lizards: cross-species chromosome mapping of cDNA reveals highly conserved synteny and gene order in the Toxicofera clade. Chromosome Res. 21, 805–819 (2013). PubMed

Meyne J. et al. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99, 3–10 (1990). PubMed

Ruiz-Herrera A., Nergadze S. G., Santagostino M. & Giulotto E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet. Genome Res. 122, 219–228 (2008). PubMed

Hebert P. D. N. & Gregory T. R. The promise of DNA barcoding for taxonomy. Syst. Biol. 54, 852–859 (2005). PubMed

Hawlitschek O., Nagy Z. T., Berger J. & Glaw F. Reliable DNA barcoding performance proved for species and island populations of comoran squamate reptiles. PLoS One 8, e73368 (2013). PubMed PMC

Jeong T. J. et al. DNA barcode reference data for the Korean herpetofauna and their applications. Mol. Ecol. Resour. 13, 1019–1032 (2013). PubMed

Murphy R. W. et al. Cold Code: the global initiative to DNA barcode amphibians and nonavian reptiles. Mol. Ecol. Resour. 13, 161–167 (2013).

Glaw F. et al. A new species of nocturnal gecko (Paroedura) from karstic limestone in northern Madagascar. Zoosystematics Evol. 90, 249–259 (2014).

Glaw F. & Vences M. A Field Guide to the Amphibians and Reptiles of Madagascar. (Vences & Glaw Verlags GbR: Köln, 2007).

Gamble T. A review of sex determining mechanisms in geckos (Gekkota: Squamata). Sex Dev. 4, 88–103 (2010). PubMed PMC

Hebert P. D. N., Cywinska A., Ball S. L. & deWaard J. R. Biological identifications through DNA barcodes. Proc. Biol. Sci. 270, 313–321 (2003). PubMed PMC

Folmer O. et al. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994). PubMed

Thompson J. D., Higgins D. G. & Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994). PubMed PMC

Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98 (1999).

Librado P. & Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009). PubMed

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013). PubMed PMC

Sumner A. T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75, 304–306 (1972). PubMed

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. 19, 4780 (1991). PubMed PMC

Endow S. A. Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics 100, 375–385 (1982). PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Heteromorphic ZZ/ZW sex chromosomes sharing gene content with mammalian XX/XY are conserved in Madagascan chameleons of the genus Furcifer

. 2024 Feb 28 ; 14 (1) : 4898. [epub] 20240228

Madagascar Leaf-Tail Geckos (Uroplatus spp.) Share Independently Evolved Differentiated ZZ/ZW Sex Chromosomes

. 2023 Jan 09 ; 12 (2) : . [epub] 20230109

ZZ/ZW Sex Chromosomes in the Madagascar Girdled Lizard, Zonosaurus madagascariensis (Squamata: Gerrhosauridae)

. 2022 Dec 29 ; 14 (1) : . [epub] 20221229

Cytogenetic Analysis of the Members of the Snake Genera Cylindrophis, Eryx, Python, and Tropidophis

. 2022 Jul 01 ; 13 (7) : . [epub] 20220701

Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?

. 2021 Sep 13 ; 376 (1833) : 20200108. [epub] 20210726

Are Geckos Special in Sex Determination? Independently Evolved Differentiated ZZ/ZW Sex Chromosomes in Carphodactylid Geckos

. 2021 Jul 06 ; 13 (7) : .

Cytogenetic Evidence for Sex Chromosomes and Karyotype Evolution in Anguimorphan Lizards

. 2021 Jun 28 ; 10 (7) : . [epub] 20210628

With or Without W? Molecular and Cytogenetic Markers are Not Sufficient for Identification of Environmentally-Induced Sex Reversal in the Bearded Dragon

. 2021 ; 15 (4) : 272-281. [epub] 20210323

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

. 2021 Jan 27 ; 288 (1943) : 20202139. [epub] 20210120

Interstitial Telomeric Repeats Are Rare in Turtles

. 2020 Jun 16 ; 11 (6) : . [epub] 20200616

Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae)

. 2020 Mar 09 ; 10 (1) : 4276. [epub] 20200309

ZZ/ZW Sex Determination with Multiple Neo-Sex Chromosomes is Common in Madagascan Chameleons of the Genus Furcifer (Reptilia: Chamaeleonidae)

. 2019 Dec 06 ; 10 (12) : . [epub] 20191206

Cytogenetic Analysis Did Not Reveal Differentiated Sex Chromosomes in Ten Species of Boas and Pythons (Reptilia: Serpentes)

. 2019 Nov 15 ; 10 (11) : . [epub] 20191115

Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards

. 2019 May 24 ; 9 (1) : 7832. [epub] 20190524

Turtles of the genera Geoemyda and Pangshura (Testudines: Geoemydidae) lack differentiated sex chromosomes: the end of a 40-year error cascade for Pangshura

. 2019 ; 7 () : e6241. [epub] 20190206

Evolutionary insight on localization of 18S, 28S rDNA genes on homologous chromosomes in Primates genomes

. 2018 ; 12 (1) : 27-40. [epub] 20180124

Evolutionary Dynamics of the W Chromosome in Caenophidian Snakes

. 2017 Dec 28 ; 9 (1) : . [epub] 20171228

Evolution of Karyotypes in Chameleons

. 2017 Dec 12 ; 8 (12) : . [epub] 20171212

Evolutionary stability of sex chromosomes in snakes

. 2015 Dec 22 ; 282 (1821) : 20151992.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...