Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Cytogenet Genome Res 2015;147:48-54
(DOI:10.1159/000441646)

Differentiation of Sex Chromosomes and Karyotype Characterisation in the Dragonsnake Xenodermus javanicus (Squamata: Xenodermatidae)

Rovatsos M.a · Johnson Pokorná M.a, b · Kratochvíl L.a

Author affiliations

aDepartment of Ecology, Faculty of Science, Charles University in Prague, Prague, and bInstitute of Animal Physiology and Genetics, The Czech Academy of Sciences, Liběchov, Czech Republic

Corresponding Author

Lukáš Kratochvíl

Department of Ecology, Faculty of Science

Charles University in Prague

CZ-128 44 Prague (Czech Republic)

E-Mail lukas.kratochvil@natur.cuni.cz

Do you have an account?

Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



Abstract

Highly differentiated heteromorphic ZZ/ZW sex chromosomes with a heterochromatic W are a basic principle among advanced snakes of the lineage Colubroidea, while other snake lineages generally lack these characteristics. For the first time, we cytogenetically examined the dragonsnake, Xenodermus javanicus, a member of the family Xenodermatidae, which is phylogenetically nested between snake lineages with and without differentiated sex chromosomes. Although most snakes have a karyotype with a stable chromosomal number of 2n = 36, the dragonsnake has an unusual, derived karyotype with 2n = 32 chromosomes. We found that heteromorphic ZZ/ZW sex chromosomes with a heterochromatic W are present in the dragonsnake, which suggests that the emergence of a highly differentiated W sex chromosome within snakes predates the split of Xenodermatidae and the clade including families Pareatidae, Viperidae, Homalopsidae, Lamprophiidae, Elapidae, and Colubridae. Although accumulations of interstitial telomeric sequences have not been previously reported in snakes, by using FISH with a telomeric probe we discovered them in 6 pairs of autosomes as well as in the W sex chromosome of the dragonsnake. Similarly to advanced snakes, the sex chromosomes of the dragonsnake have a significant accumulation of repeats containing a (GATA)n sequence. The results facilitate the dating of the differentiation of sex chromosomes within snakes back to the split between Xenodermatidae and other advanced snakes, i.e. around 40-75 mya.

© 2015 S. Karger AG, Basel


References

  1. Aldridge RD, Sever DM (eds): Reproductive Biology and Phylogeny of Snakes (Science Publishers Enfield, New Hampshire 2011).
  2. Azzalin CM, Nergadze SG, Giulotto E: Human intrachromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110:75-82 (2001).
  3. Beçak W, Beçak ML: Cytotaxonomy and chromosomal evolution in Serpentes. Cytogenetics 8:247-262 (1969).
  4. Britton-Davidian J, Cazaux B, Catalan J: Chromosomal dynamics of nucleolar organizer regions (NORs) in the house mouse: micro-evolutionary insights. Heredity 108:68-74 (2012).
  5. Endow SA: Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics 100:375-385 (1982).
    External Resources
  6. Epplen JT, McCarrey JR, Sutou S, Ohno S: Base sequence of a cloned snake W-chromosome DNA fragment and identification of a male-specific putative mRNA in the mouse. Proc Natl Acad Sci USA 79:3798-3802 (1982).
  7. Gornung E: Twenty years of physical mapping of major ribosomal RNA genes across the teleosts: a review of research. Cytogenet Genome Res 141:90-102 (2013).
  8. Gornung E, Castiglia R, Rovatsos M, Marchal JA, Díaz de la Guardia-Quiles R, Sanchez A: Comparative cytogenetic study of two sister species of Iberian ground voles, Microtus (Terricola) duodecimcostatus and M. (T.) lusitanicus (Rodentia, Cricetidae). Cytogenet Genome Res 132:144-150 (2011).
  9. Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95-98 (1999).
  10. Heise PJ, Maxson LR, Dowling HG, Hedges SB: Higher-level snake phylogeny inferred from mitochondrial DNA sequences of 12s rRNA and 16s rRNA genes. Mol Biol Evol 12:259-265 (1995).
    External Resources
  11. Ijdo JW, Wells RA, Baldini A, Reeders ST: Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780 (1991).
  12. 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).
  13. Jones KW, Singh L: Snakes and evolution of sex chromosomes. Trends Genet 1:55-61 (1985).
    External Resources
  14. Kelly CMR, Barker NP, Villet MH: Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes. Syst Biol 52:439-459 (2003).
  15. 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 22:441-452 (2014).
  16. Lee C, Sasi R, Lin CC: Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs. Cytogenet Cell Genet 63:156-159 (1993).
  17. Lee MSY, Hugall AF, Lawson R, Scanlon JD: Phylogeny of snakes (Serpentes): combining morphological and molecular data in likelihood, Bayesian and parsimony analyses. Syst Biodiv 5:371-389 (2007).
    External Resources
  18. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452 (2009).
  19. Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, et al: Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci USA 103:18190-18195 (2006).
  20. Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, et al: Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99:3-10 (1990).
  21. Mulcahy DG, Noonan BP, Moss T, Townsend TM, Reeder TW, et al: Estimating divergence dates and evaluating dating methods using phylogenomic and mitochondrial data in squamate reptiles. Mol Phylogenet Evol 65:974-991 (2012).
  22. Nagy ZT, 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).
  23. Oguiura N, Ferrarezzi H, Batistic RF: Cytogenetics and molecular data in snakes: a phylogenetic approach. Cytogenet Genome Res 127:128-142 (2009).
  24. Ohno S: Sex Chromosomes and Sex Linked Genes (Springer, Berlin 1967).
  25. Olmo E, Signorino G: Chromorep: A Reptiles Chromosomes Database, http://chromorep.univpm.it (2015).
  26. O'Meally D, Patel HR, Stiglec R, Sarre SD, Georges A, et al: Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res 18:787-800 (2010).
  27. Pellegrino KCM, Rodrigues MT, Yonenaga-Yassuda Y: Chromosomal evolution in the Brazilian lizards of genus Leposoma (Squamata, Gymnophthalmidae) from Amazon and Atlantic rain forests: banding patterns and FISH of telomeric sequences. Hereditas 131:15-21 (1999).
  28. 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).
    External Resources
  29. 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 (2011).
  30. 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).
  31. Pyron RA, Burbrink FT: Extinction, ecological opportunity, and the origins of global snake diversity. Evolution 66:163-178 (2012).
  32. Pyron RA, Burbrink FT, Colli GR, de Oca ANM, Vitt LJ, et al: The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58:329-42 (2011).
  33. Pyron RA, Burbrink FT, Wiens JJ: A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93 (2013).
  34. Pyron RA, Hendry CR, Chou VM, Lemmon EM, Lemmon AR, Burbrink FT: Effectiveness of phylogenomic data and coalescent species-tree methods for resolving difficult nodes in the phylogeny of advanced snakes (Serpentes: Caenophidia). Mol Phylogenet Evol 81:221-231 (2014).
  35. Ray-Chaudhuri SP, Singh L, Sharma T: Evolution of sex chromosomes and formation of W chromatin in snakes. Chromosoma 33: 239-251 (1971).
  36. Rovatsos MT, Marchal JA, Romero-Fernández I, Fernández FJ, et al: Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res 19:869-882 (2011).
  37. Rovatsos MT, Marchal JA, Romero-Fernández I, Cano-Linares M, Fernández FJ, et al: Molecular and physical characterization of the complex pericentromeric heterochromatin of the vole species Microtus thomasi. Cytogenet Genome Res 144:131-141 (2014).
  38. 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 (2015a).
  39. Rovatsos M, Kratochvíl L, Altmanová M, Johnson Pokorná M: Interstitial telomeric motifs in squamate reptiles: when the exceptions outnumber the rule. PLoS One 10:e0134985 (2015b).
  40. Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E: Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res 122:219-228 (2008).
  41. Sharma GP, Nakhasi U: Chromosomal polymorphism in three species of Indian snakes. Cytobios 24:167-179 (1979).
    External Resources
  42. Sharma GP, Nakhasi U: Karyological studies on six species of Indian snakes (Colubridae: Reptilia). Cytobios 27:177-192 (1980).
    External Resources
  43. Singh L, Jones KW: Sex reversal in mouse (Mus musculus) is caused by a recurrent non-reciprocal crossover involving the X and an aberrant Y chromosome. Cell 28:205-216 (1982).
  44. Srikulnath K, Matsubara K, Uno Y, Thongpan A, Suputtitada S, et al: Karyological characterization of the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Squamata) by molecular cytogenetic approach. Cytogenet Genome Res 125:213-223 (2009).
  45. Subramanian S, Mishra RK, Singh L: Genome-wide analysis of Bkm sequences (GATA repeats): predominant association with sex chromosomes and potential role in higher order chromatin organization and function. Bioinformatics 19:681-685 (2003).
  46. Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304-306 (1972).
  47. 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).
  48. Teynie A, David P, Lottier A, Le MD, Vidal N, Nguyen TQ: A new genus and species of xenodermatid snake (Squamata: Caenophidia: Xenodermatidae) from northern Lao People's Democratic Republic. Zootaxa 3926:523-540 (2015).
  49. Thompson JD, Higgins DG, Gibson TJ: ClustalW: 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).
  50. Uetz, P, Hošek J: The Reptile Database, http://www.reptile-database.org, accessed April 21, 2015.
  51. 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 11:e1001643 (2013).
  52. Wiens JJ, Kuczynski CA, Smith SA, Mulcahy DG, Sites JW, et al: Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Syst Biol 57:420-431 (2008).
  53. Wogan G, Grismer L, Chan-Ard T: Xenodermus javanicus. The IUCN Red List of Threatened Species, www.iucnredlist.org, accessed April 23, 2015.

Article / Publication Details

First-Page Preview
Abstract of Original Article

Received: October 01, 2015
Published online: November 18, 2015

Number of Print Pages: 7
Number of Figures: 2
Number of Tables: 0

ISSN: 1424-8581 (Print)
eISSN: 1424-859X (Online)

For additional information: https://www.karger.com/CGR