Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): differentiation of sex and neo-sex chromosomes
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
26286647
PubMed Central
PMC4541320
DOI
10.1038/srep13196
PII: srep13196
Knihovny.cz E-zdroje
- MeSH
- haplotypy genetika MeSH
- ještěři genetika MeSH
- karyotypizace MeSH
- pigmentace genetika MeSH
- pohlavní chromozomy genetika MeSH
- procesy určující pohlaví genetika MeSH
- respirační komplex IV genetika MeSH
- sekvence nukleotidů MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- respirační komplex IV MeSH
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.
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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
Cytogenetic Analysis of the Members of the Snake Genera Cylindrophis, Eryx, Python, and Tropidophis
Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?
Cytogenetic Evidence for Sex Chromosomes and Karyotype Evolution in Anguimorphan Lizards
Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation
Interstitial Telomeric Repeats Are Rare in Turtles
Evolutionary Dynamics of the W Chromosome in Caenophidian Snakes
Evolution of Karyotypes in Chameleons
Evolutionary stability of sex chromosomes in snakes