Molecular Cytogenetic Characterization of the Sicilian Endemic Pond Turtle Emys trinacris and the Yellow-Bellied Slider Trachemys scripta scripta (Testudines, Emydidae)
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32630506
PubMed Central
PMC7348936
DOI
10.3390/genes11060702
PII: genes11060702
Knihovny.cz E-zdroje
- Klíčová slova
- Emys trinacris, FISH, Trachemys scripta scripta, karyotype, rDNA, telomeric sequences,
- MeSH
- cytogenetika metody MeSH
- hybridizace in situ fluorescenční metody MeSH
- karyotyp * MeSH
- molekulární evoluce * MeSH
- ribozomální DNA genetika MeSH
- telomery genetika MeSH
- želvy genetika MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
Turtles, a speciose group consisting of more than 300 species, demonstrate karyotypes with diploid chromosome numbers ranging from 2n = 26 to 2n = 68. However, cytogenetic analyses have been conducted only to 1/3rd of the turtle species, often limited to conventional staining methods. In order to expand our knowledge of the karyotype evolution in turtles, we examined the topology of the (TTAGGG)n telomeric repeats and the rDNA loci by fluorescence in situ hybridization (FISH) on the karyotypes of two emydids: the Sicilian pond turtle, Emys trinacris, and the yellow-bellied slider, Trachemys scripta scripta (family Emydidae). Furthermore, AT-rich and GC-rich chromosome regions were detected by DAPI and CMA3 stains, respectively. The cytogenetic analysis revealed that telomeric sequences are restricted to the terminal ends of all chromosomes and the rDNA loci are localized in one pair of microchromosomes in both species. The karyotype of the Sicilian endemic E. trinacris with diploid number 2n = 50, consisting of 13 pairs of macrochromosomes and 12 pairs of microchromosomes, is presented here for first time. Our comparative examination revealed similar cytogenetic features in Emys trinacris and the closely related E. orbicularis, as well as to other previously studied emydid species, demonstrating a low rate of karyotype evolution, as chromosomal rearrangements are rather infrequent in this group of turtles.
Zobrazit více v PubMed
Uetz P., Freed P., Hošek J. The Reptile Database. [(accessed on 28 May 2020)]; Available online: http://www.reptile-database.org.
Parham J.F., Papenfuss T.J., van Dijk P.P., Wilson B.S., Marte C., Rodriguez-Schettino L., Simison W.B. Genetic introgression and hybridization in Antillean freshwater turtles (Trachemys) revealed by coalescent analyses of mitochondrial and cloned nuclear markers. Mol. Phylogenet. Evol. 2013;67:176–187. doi: 10.1016/j.ympev.2013.01.004. PubMed DOI
Parham J.F., Papenfuss T.J., Buskirk J.R., Parra-Olea G., Chen J.Y., Simison W.B. Trachemys ornata or not ornata: Reassessment of a taxonomic revision for Mexican Trachemys. Proc. Calif. Acad. Sci. 2015;62:359–367.
Rogner M. European Pond Turtle: Emys Orbicularis. Chelonian Library, Edition Chimaira; Frankfurt, Germany: 2009.
Gaffney E.S., Meylan P.A. In: A Phylogeny of Turtles in: The Phylogeny and Classification of Tetrapods. Benton M.J., editor. Clarendon; Oxford, UK: 1988. pp. 157–219.
Marrone F., Sacco F., Arizza V., Arculeo M. Amendment of the type locality of the endemic Sicilian pond turtle Emys trinacris, Fritz et al. 2005, with some notes on the highest altitude reached by the species (Testudines, Emydidae) Acta Herpetol. 2016;11:63–65.
Vamberger M., Fritz U. Big data can cause big mistakes: Using the Societas Europaea Herpetologica atlas by Sillero et al. (2014), the distribution of Emys orbicularis will be misunderstood. Biologia. 2018;73:281–283. doi: 10.2478/s11756-018-0033-6. DOI
Feldman C.R., Parham J.F. Molecular phylogenetics of emydine turtles: Taxonomic revision and the evolution of shell kinesis. Mol. Phylogenet. Evol. 2002;22:388–398. doi: 10.1006/mpev.2001.1070. PubMed DOI
Fritz U., Schmidt C., Ernst C.H. Competing generic concepts for Blanding’s, Pacific and European pond turtles (Emydoidea, Actinemys and Emys)—Which is best? Zootaxa. 2011;2791:41–53. doi: 10.11646/zootaxa.2791.1.3. DOI
Seidel M.E., Ernst C.H. A systematic review of the turtle family Emydidae. Vertebr. Zool. 2017;67:1–122.
D’Angelo S., Pennisi M.G., Lo Valvo M., Fritz U. Variation of Sicilian pond turtles, Emys trinacris—What makes a species cryptic? Amphib-Reptil. 2006;27:513–529. doi: 10.1163/156853806778877095. DOI
Arizza V., Russo D., Marrone F., Sacco F., Arculeo M. Morphological characterization of the blood cells in the endangered endemic pond turtle, Emys trinacris (Testudines: Emydidae) Ital. J. Zool. 2014;81:344–353. doi: 10.1080/11250003.2014.938371. DOI
Fritz U., Fattizzo T., Guicking D., Tripepi S., Pennisi M.G., Lenk P., Joger U., Wink M. A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys. Zool. Scr. 2005;34:351–371. doi: 10.1111/j.1463-6409.2005.00188.x. DOI
Stuckas H., Velo-Antón G., Fahd S., Kalboussi M., Rouag R., Arculeo M., Marrone F., Sacco F., Vamberger M., Fritz U. Where are you from, stranger? The enigmatic biogeography of North African pond turtles (Emys orbicularis) Org. Divers. Evol. 2014;14:295–306. doi: 10.1007/s13127-014-0168-4. DOI
Vamberger M., Stuckas H., Sacco F., D’Angelo S., Arculeo M., Cheylan M., Corti C., Lo Valvo M., Marrone F., Wink M., et al. Differences in gene flow in a twofold secondary contact zone of pond turtles in southern Italy (Testudines: Emydidae: Emys orbicularis galloitalica, E. o. hellenica, E. trinacris) Zool. Scr. 2015;44:233–249. doi: 10.1111/zsc.12102. DOI
Marrone F., Sacco F., Kehlmaier C., Arizza V., Arculeo M. Some like it cold: The glossiphoniid parasites of the Sicilian endemic pond turtle Emys trinacris (Testudines, Emydidae), an example of ‘parasite inertia’? J. Zool. Syst. Evol. Res. 2016;54:60–66. doi: 10.1111/jzs.12117. DOI
Olmo E., Signorino G.G. Chromorep: A Reptile Chromosomes Database. [(accessed on 14 April 2020)]; Available online: http://chromorep.univpm.it.
Bickham J.W., Baker R.J. Chromosome homology and evolution of emydid turtles. Chromosoma. 1976;54:201–219. doi: 10.1007/BF00293451. PubMed DOI
Bickham J.W., Carr J.L. Taxonomy and phylogeny of the higher categories of Cryptodiran turtles based on a cladistics analysis of chromosomal data. Copeia. 1983;4:918–932. doi: 10.2307/1445093. DOI
Cleiton F., Giuliano-Caetano L. Cytogenetic characterization of two turtle species: Trachemys dorbigni and Trachemys scripta elegans. Caryologia. 2008;61:253–257. doi: 10.1080/00087114.2008.10589637. DOI
Iannucci A., Svartman M., Bellavita M., Chelazzi G., Stanyon R., Ciofi C. Insights into emydid turtle cytogenetics: The european pond turtle as a model species. Cytogenet. Genome Res. 2019;157:166–171. doi: 10.1159/000495833. PubMed DOI
Montiel E.E., Badenhorst D., Lee L.S., Literman R., Trifonov V., Valenzuela N. Cytogenetic insights into the evolution of chromosomes and sex determination reveal striking homology of turtle sex chromosomes to amphibian autosomes. Cytogenet. Genome Res. 2016;148:292–304. doi: 10.1159/000447478. PubMed DOI
Montiel E.E., Badenhorst D., Tamplin J., Burke R., Valenzuela N. Discovery of youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma. 2017;126:105–113. doi: 10.1007/s00412-016-0576-7. PubMed DOI
Valenzuela N., Badenhorst D., Montiel E.E., Literman R. Molecular cytogenetic search for cryptic sex chromosomes in painted turtles Chrysemys picta. Cytogenet. Genome Res. 2014;144:39–46. doi: 10.1159/000366076. PubMed DOI
Martinez P.A., Boeris J.M., Sánchez J., Pastori M.C., Bolzán A.D., Ledesma M.A. Karyotypic characterization of Trachemys dorbigni (Testudines: Emydidae) and Chelonoidis (Geochelone) donosobarrosi (Testudines: Testudinidae), two species of cryptodiran turtles from Argentina. Genetica. 2009;137:277–283. doi: 10.1007/s10709-009-9377-8. PubMed DOI
Kasai F., O’Brien P.C.M., Martin S., Ferguson-Smith M.A. Extensive homology of chicken macrochromosomes in the karyotypes of Trachemys scripta elegans and Crocodylus niloticus revealed by chromosome painting despite long divergence times. Cytogenet. Genome Res. 2012;136:303–307. doi: 10.1159/000338111. PubMed DOI
Badenhorst D., Hillier L.W., Literman R., Montiel E.E., Radhakrishnan S., Shen Y., Minx P., Janes D.E., Warren W.C., Edwards S.V., et al. Physical mapping and refinement of the painted turtle genome (Chrysemys picta) inform amniote genome evolution and challenge turtle-bird chromosomal conservation. Genome Biol. Evol. 2015;7:2038–2050. doi: 10.1093/gbe/evv119. PubMed DOI PMC
Picone B., Dumas F., Stanyon R., Lannino A., Bigoni F., Privitera O., Sineo L. Exploring evolution in 298 Ceboidea (Platyrrhini, Primates) by Williams-Beuren Probe (HSA 7q11.23) chromosome mapping. Folia Primatol. 2008;79:417–427. doi: 10.1159/000151236. PubMed DOI
Dumas F., Houck M., Bigoni F., Perelman P., Romanenko S., Stanyon R. Chromosome painting of the.pygmy tree shrew shows that no derived cytogenetic traits link primates and scandentia. Cytogenet. Genome Res. 2012;136:175–179. doi: 10.1159/000336976. PubMed DOI
Dumas F., Stanyon R., Sineo L., Stone G., Bigoni F. Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting. BMC Evol. Boil. 2007;7:S11. doi: 10.1186/1471-2148-7-S2-S11. PubMed DOI PMC
Dumas F., Sineo L. Chromosomal dynamics in platyrrhinae by mapping BACs probes. J. Biol. Res. 2012;LXXXV:299–301.
Dumas F., Sineo L. Chromosomal dynamics in Cercopithecini studied by Williams-Beuren probe mapping. Caryologia. 2010;63:435–442.
Dumas F., Sineo L. The evolution of human synteny 4 by mapping sub-chromosomal specific probes in Primates. Caryologia. 2014;67:281–291. doi: 10.1080/0144235X.2014.974357. DOI
Scardino R., Milioto V., Proskuryakova A.A., Serdyukova N.A., Perelman P.L., Dumas F. Evolution of the human chromosome 13 synteny: Evolutionary rearrangements, plasticity, human disease genes and cancer breakpoints. Genes. 2020;11:383. doi: 10.3390/genes11040383. PubMed DOI PMC
Dumas F., Sineo L., Ishida T. Taxonomic identification of Aotus (Platyrrhinae) through cytogenetics | Identificazione tassonomica di Aotus (Platyrrhinae) mediante la citogenetica. J. Biol. Res. 2015;88:65–66.
Dumas F., Mazzoleni S. Neotropical primate evolution and phylogenetic reconstruction using chromosomal data. Eur. Zoöl. J. 2017;84:1–18. doi: 10.1080/11250003.2016.1260655. DOI
Rovatsos M., Kratochvíl L., Altmanová M., Johnson Pokorná M. Interstitial telomeric motifs in squamate reptiles: When the exceptions outnumber the rule. PLoS ONE. 2015;10:e0134985. doi: 10.1371/journal.pone.0134985. PubMed DOI PMC
Matsubara K., Uno Y., Srikulnath K., Matsuda Y., Miller E., Olsson M. No interstitial telomeres on autosomes but remarkable amplification of telomeric repeats on the W sex chromosome in the sand lizard (Lacerta agilis) J. Hered. 2015;106:753–757. doi: 10.1093/jhered/esv083. PubMed DOI
Dumas F., Cuttaia H., Sineo L. Chromosomal distribution of interstitial telomeric sequences in nine neotropical primates (Platyrrhini): Possible implications in evolution and phylogeny. J. Zoöl. Syst. Evol. Res. 2016;54:226–236. doi: 10.1111/jzs.12131. DOI
Mazzoleni S., Schillaci O., Sineo L., Dumas F. Distribution of interstitial telomeric sequences in primates and the pygmy tree shrew (Scandentia) Cytogenet. Genome Res. 2017;151:141–150. doi: 10.1159/000467634. PubMed DOI
Mazzoleni S., Rovatsos M., Schillaci O., Dumas F. Evolutionary insight on localization of 18S, 28S rDNA genes on homologous chromosomes in Primates genomes. Comp. Cytogenet. 2018;12:27–40. doi: 10.3897/compcytogen.v12i1.19381. PubMed DOI PMC
Milioto V., Vlah S., Mazzoleni S., Rovatsos M., Dumas F. Chromosomal localization of 18S-28S rDNA and (TTAGGG)n sequences in two south african dormice of the genus Graphiurus (Rodentia: Gliridae) Cytogenet. Genome Res. 2019;158:145–151. doi: 10.1159/000500985. PubMed DOI
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
Mazzoleni S., Augstenová B., Clemente L., Auer M., Fritz U., Praschag P., Protiva T., Velenský P., Kratochvíl L., Rovatsos M. Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae) Sci. Rep. 2020;10:1–11. doi: 10.1038/s41598-020-61116-w. PubMed DOI PMC
Meyne J., Ratliff R.L., Moyzis R.K. Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc. Natl. Acad. Sci. USA. 1989;86:7049–7053. doi: 10.1073/pnas.86.18.7049. PubMed DOI PMC
Meyne J., Baker R.J., Hobart H.H., Hsu T.C., Ryder O.A., Ward O.G., Wiley J.E., Wurster-Hill D.H., Yates T.L., Moyzis R.K. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma. 1990;99:3–10. doi: 10.1007/BF01737283. PubMed DOI
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. 2008;122:219–228. doi: 10.1159/000167807. PubMed DOI
Ficetola G.F., Scali S. Atti VIII Congresso Nazionale Societas Herpetologica Italica. Ianieri Edizioni; Pescara, Italy: 2010. Invasive amphibians and reptiles in Italy; pp. 335–340.
Redrobe S., MacDonald J. Sample collection and clinical pathology of reptiles. Vet. Clin. N. Am. Exot. Anim. Pract. 1999;2:709–730. doi: 10.1016/S1094-9194(17)30118-4. PubMed DOI
Naselli-Flores L., Marrone F. Different invasibility of permanent and temporary waterbodies in a semiarid Mediterranean Island. Inland Waters. 2019;9:41–421. doi: 10.1080/20442041.2019.1653110. DOI
Mazzoleni S., Augstenová B., Clemente L., Auer M., Fritz U., Praschag P., Protiva T., Velenský P., Kratochvíl L., Rovatsos M. 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;7:e6241. doi: 10.7717/peerj.6241. PubMed DOI PMC
Belaiba E., Marrone F., Vecchioni L., Bahri-Sfar L., Arculeo M. An exhaustive phylogeny of the combtooth blenny genus Salaria (Pisces, Blenniidae) shows introgressive hybridization and lack of reciprocal mtDNA monophyly between the marine species Salaria basilisca and Salaria pavo. Mol. Phylogenet. Evol. 2019;135:210–221. doi: 10.1016/j.ympev.2019.02.026. PubMed DOI
Kasai F., O’Brien P.C.M., Ferguson-Smith M.A. Reassessment of genome size in turtle and crocodile based on chromosome measurement by flow karyotyping: Close similarity to chicken. Biol Lett. 2012;8:631–635. doi: 10.1098/rsbl.2012.0141. PubMed DOI PMC
Olmo E. Trends in the evolution of reptilian chromosomes. Integr. Comp. Biol. 2008;48:486–493. doi: 10.1093/icb/icn049. PubMed DOI
Bista B., Valenzuela N. Turtle insights into the evolution of the reptilian karyotype and the genomic architecture of sex determination. Genes. 2020;11:416. doi: 10.3390/genes11040416. PubMed DOI PMC
Vamberger M., Ihlow F., Asztalos M., Dawson J.E., Jasinski S.E., Praschag P., Fritz U. So different, yet so alike: North American slider turtles (Trachemys scripta) Vertebr. Zool. 2020;70:87–96.