Cytogenetic Analysis of the Asian Box Turtles of the Genus Cuora (Testudines, Geoemydidae)
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33503936
PubMed Central
PMC7911423
DOI
10.3390/genes12020156
PII: genes12020156
Knihovny.cz E-zdroje
- Klíčová slova
- C-banding, Cuora, FISH, Geoemydidae, evolution, heterochromatin, karyotype, microsatellites, rDNA, telomeres,
- MeSH
- cytogenetické vyšetření * MeSH
- fylogeneze MeSH
- hybridizace in situ fluorescenční MeSH
- karyotyp MeSH
- mikrosatelitní repetice MeSH
- molekulární evoluce MeSH
- pruhování chromozomů MeSH
- ribozomální DNA genetika MeSH
- taxonomické DNA čárové kódování MeSH
- telomery MeSH
- želvy klasifikace genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
The Asian box turtle genus Cuora currently comprises 13 species with a wide distribution in Southeast Asia, including China and the islands of Indonesia and Philippines. The populations of these species are rapidly declining due to human pressure, including pollution, habitat loss, and harvesting for food consumption. Notably, the IUCN Red List identifies almost all species of the genus Cuora as Endangered (EN) or Critically Endangered (CR). In this study, we explore the karyotypes of 10 Cuora species with conventional (Giemsa staining, C-banding, karyogram reconstruction) and molecular cytogenetic methods (in situ hybridization with probes for rDNA loci and telomeric repeats). Our study reveals a diploid chromosome number of 2n = 52 chromosomes in all studied species, with karyotypes of similar chromosomal morphology. In all examined species, rDNA loci are detected at a single medium-sized chromosome pair and the telomeric repeats are restricted to the expected terminal position across all chromosomes. In contrast to a previous report, sex chromosomes are neither detected in Cuoragalbinifrons nor in any other species. Therefore, we assume that these turtles have either environmental sex determination or genotypic sex determination with poorly differentiated sex chromosomes. The conservation of genome organization could explain the numerous observed cases of interspecific hybridization both within the genus Cuora and across geoemydid turtles.
Allwetterzoo Münster 48161 Münster Germany
Department of Ecology Faculty of Science Charles University 12844 Prague Czech Republic
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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
Clemente L., Mazzoleni S., Pensabene Bellavia E., Augstenová B., Auer M., Praschag P., Protiva T., Velenský P., Wagner P., Fritz U., et al. Interstitial telomeric repeats are rare in turtles. Genes. 2020;11:657. doi: 10.3390/genes11060657. PubMed DOI PMC
Olmo E., Signorino G.G. Chromorep: A Reptile Chromosomes Database. [(accessed on 14 April 2020)]; Available online: http://chromorep.univpm.it.
Rhodin A.G.J., Stanford C.B., Van Dijk P.P., Eisemberg C., Luiselli L., Mittermeier R.A., Hudson R., Horne B.D., Goode E.V., Kuchling G., et al. Global conservation status of turtles and tortoises (order Testudines) Chelonian Conserv. Biol. 2018;17:135–161. doi: 10.2744/CCB-1348.1. DOI
Farkas B., Ziegler T., Pham C.T., Ong A.V., Fritz U. A new species of Pelodiscus from northeastern Indochina (Testudines, Trionychidae) ZooKeys. 2019;824:71–84. doi: 10.3897/zookeys.824.31376. PubMed DOI PMC
Loc-Barragán J.A., Reyes-Velasco J., Woolrich-Pina G.A., Grunwald C.I., de Anaya M.V., Rangel-Mendoza J.A., López-Luna M.A. A new species of mud turtle of genus Kinosternon (Testudines: Kinosternidae) from the Pacific coastal plain of northwestern Mexico. Zootaxa. 2020;3885:509–529. doi: 10.11646/zootaxa.4885.4.3. PubMed DOI
Vargas-Ramírez M., Caballero S., Morales-Betancourt M.A., Lasso C.A., Amaya L., Martínez J.G., das Neves Silva Viana M., Vogt R.C., Farias I.P., Hrbek T., et al. Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography. Mol. Phylogenet. Evol. 2020;148:106823. doi: 10.1016/j.ympev.2020.106823. PubMed DOI
Uetz P., Freed P., Hošek J. The Reptile Database. [(accessed on 13 April 2020)]; Available online: http://www.reptile-database.org.
Ventura K., Moreira C.N., Moretti R., Yonenaga-Yassuda Y., Rodrigues M.T. The lowest diploid number in Testudines: Banding patterns, telomeric and 45s rDNA FISH in Peltocephalus dumerilianus, 2n = 26 and FN = 52 (Pleurodira, Podocnemididae) Genet. Mol. Biol. 2014;37:61–63. doi: 10.1590/S1415-47572014000100011. PubMed DOI PMC
Cavalcante M.G., Bastos C.E.M.C., Nagamachi C.Y., Pieczarka J.C., Vicari M.R., Noronha R.C.R. Physical mapping of repetitive DNA suggests 2n reduction in Amazon turtles Podocnemis (Testudines: Podocnemididae) PLoS ONE. 2018;13:e0197536. doi: 10.1371/journal.pone.0197536. PubMed DOI PMC
Stock A.D., Burnham D.B., Hsu T.C. Giemsa banding of meiotic chromosomes with description of a procedure for cytological preparations from solid tissues. Cytogenetics. 1972;11:534–539. doi: 10.1159/000130219. PubMed DOI
Killebrew F.C. Mitotic chromosomes of turtles. IV. The Emydidae. Tex. J. Sci. 1977;29:245–253.
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
Valenzuela N., Adams D.C. Chromosome number and sex determination coevolve in turtles. Evolution. 2011;65:1808–1813. doi: 10.1111/j.1558-5646.2011.01258.x. PubMed 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
Johnson Pokorná M., Kratochvíl L. What was the ancestral sex-determining mechanism in amniote vertebrates? Biol. Rev. 2016;91:1–12. doi: 10.1111/brv.12156. PubMed DOI
Straková B., Rovatsos M., Kubička L., Kratochvíl L. Evolution of sex determination in amniotes: Did stress and sequential hermaphroditism produce environmental determination? BioEssays. 2020;42:e2000050. doi: 10.1002/bies.202000050. 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
Bull J.J., Moon R.G., Legler J.M. Male heterogamety in kinosternid turtles (genus Staurotypus) Cytogenet. Genome Res. 1974;13:419–425. doi: 10.1159/000130295. PubMed DOI
Ezaz T., Valenzuela N., Grützner F., Miura I., Georges A., Burke R.L., Graves J.A. An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosome Res. 2006;14:139–150. doi: 10.1007/s10577-006-1029-6. PubMed DOI
Martinez P.A., Ezaz T., Valenzuela N., Georges A., Marshall Graves J.A. An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: A new piece in the puzzle of sex chromosome evolution in turtles. Chromosome Res. 2008;16:815–825. doi: 10.1007/s10577-008-1228-4. PubMed DOI
Kawagoshi T., Nishida C., Matsuda Y. The origin and differentiation process of X and Y chromosomes of the black marsh turtle (Siebenrockiella crassicollis, Geoemydidae, Testudines) Chromosome Res. 2012;20:95–110. doi: 10.1007/s10577-011-9267-7. PubMed DOI
Literman R., Radhakrishnan S., Tamplin J., Burke R., Dresser C., Valenzuela N. Development of sexing primers in Glyptemys insculpta and Apalone spinifera turtles uncovers an XX/XY sex-determining system in the critically-endangered bog turtle Glyptemys muhlenbergii. Conserv. Genet. Res. 2017;9:651–658. doi: 10.1007/s12686-017-0711-7. DOI
Rovatsos M., Praschag P., Fritz U., Kratochvil L. Stable Cretaceous sex chromosomes enable molecular sexing in softshell turtles (Testudines: Trionychidae) Sci. Rep. 2017;7:42150. doi: 10.1038/srep42150. PubMed DOI PMC
Lee Y., Lin J.W., Tseng S.P., Chen T.S., Lin S.M. Human disturbance as a possible cause of genetic introgression from exotic into native Mauremys turtles. Anim. Conserv. 2019;22:556–567. doi: 10.1111/acv.12494. DOI
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;10:4276. doi: 10.1038/s41598-020-61116-w. PubMed DOI PMC
Viana P.F., Feldberg E., Cioffi M.B., de Carvalho V.T., Menezes S., Vogt R.C., Liehr T., Ezaz T. The Amazonian red side-necked turtle Rhinemys rufipes (Spix, 1824) (Testudines, Chelidae) has a GSD sex-determining mechanism with an ancient XY sex microchromosome System. Cells. 2020;9:2088. doi: 10.3390/cells9092088. PubMed DOI PMC
Sharma G.P., Kaur P., Nakhasi U. Female heterogamety in the Indian cryptodiran chelonian, Kachuga smithi Gray. In: Tiwari K.K., Srivastava C.B., editors. Dr. B.S. Chauhan Commemoration Volume. Zoological Society of India; Bhubaneshwar, Orissa, India: 1975. pp. 359–368.
Rhodin A.G.J., Iverson J.B., Bour R., Fritz U., Georges A., Shaffer H.B., Van Dijk P.P., TTWG—Turtle Taxonomy Working Group Turtles of the world: Annotated checklist and atlas of taxonomy, synonymy, distribution and conservation status (8th edition) Chelonian Res. Monogr. 2017;7:1–202.
Colston T.J., Kulkarni P., Jetz W., Pyron R.A. Phylogenetic and spatial distribution of evolutionary diversification, isolation, and threat in turtles and crocodilians (non-avian archosauromorphs) BMC Evol. Biol. 2020;20:81. doi: 10.1186/s12862-020-01642-3. PubMed DOI PMC
Bickham J.W. A cytosystematic study of turtles in the genera Clemmys, Mauremys and Sacalia. Herpetologica. 1975;31:198–204.
Bickham J., Carr J. Taxonomy and phylogeny of the higher categories of Cryptodiran turtles based on a cladistic analysis of chromosomal data. Copeia. 1983;4:918–932. doi: 10.2307/1445093. DOI
Carr J.L., Bickham J.W. Phylogenetic implications of karyotype variation in the Batagurinae (Testudines: Emydidae) Genetica. 1986;70:89–106. doi: 10.1007/BF00123580. DOI
Guo C., Nie L., Wang M. A cytogenetic study of four species of turtle from China. Acta Genet. Sin. 1995;22:40–45. PubMed
Siripiyasing P., Tanomtong A., Jumrusthanasan S., Patawang I., Phimphan S., Sanoamuang L.O. First cytogenetic study of Malayan snail-eating turtle, Malayemys macrocephala (Testudines, Geoemydidae) in Thailand. Cytologia. 2013;78:125–132. doi: 10.1508/cytologia.78.125. DOI
Cavalcante M.G., Souza L.F., Vicari M.R., de Bastos C., de Sousa J.V., Nagamachi C.Y., Pieczarka J.C., Martins C., Noronha R. Molecular cytogenetics characterization of Rhinoclemmys punctularia (Testudines, Geoemydidae) and description of a Gypsy-H3 association in its genome. Gene. 2020;738:144477. doi: 10.1016/j.gene.2020.144477. PubMed DOI
Yadollahvand R., Kami H.G., Kalbassi M.R. Cytogenetic characterisation of the Caspian Pond Turtle, Mauremys caspica in Golestan and Mazandaran provinces, Iran (Reptilia: Testudines) Zool. Middle East. 2013;59:214–219. doi: 10.1080/09397140.2013.841426. DOI
Ewert M.A., Etchberger C.R., Nelson C.E. Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates. In: Valenzuela N., Lance V.A., editors. Temperature-Dependent Sex Determination in Vertebrates. Smithsonian Institution Press; Washington, DC, USA: 2004. pp. 21–32.
Farrell R. TSA Turtle Survival Alliance. 2007. [(accessed on 17 December 2020)]. Temperature sex determination (TSD) project for the yellow-margined box turtle, Cuora flavomarginata; pp. 1–46. Available online: https://turtlesurvival.org.
Stanford C.B., Iverson J.B., Rhodin A.G., van Dijk P.P., Mittermeier R.A., Kuchling G., Berry K.H., Bertolero A., Bjorndal K.A., Blanck T.E., et al. Turtles and tortoises are in trouble. Curr. Biol. 2020;30:R721–R735. doi: 10.1016/j.cub.2020.04.088. PubMed DOI
The IUCN Red List of Threatened Species. [(accessed on 17 December 2020)]; Available online: https://www.iucnredlist.org/
Gorman G.C. The chromosomes of the Reptilia, a cytotaxonomic interpretation. In: Chiarelli A.B., Capanna E., editors. Cytotaxonomy and Vertebrate Evolution. Acad. Press; London, UK: New York, NY, USA: 1973. pp. 347–424.
Burbrink F.T., Lawson R., Slowinski J.B. Mitochondrial DNA phylogeography of the polytypic North American ratsnake (Elaphe obsoleta): A critique of the subspecies concept. Evolution. 2000;54:2107–2118. doi: 10.1111/j.0014-3820.2000.tb01253.x. PubMed DOI
FinchTV v1.4.0. [(accessed on 25 December 2020)]; Available online: https://digitalworldbiology.com/FinchTV.
Geneious Prime 2020. [(accessed on 25 December 2020)]; Available online: https://www.geneious.com.
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Sumner A.T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 1972;75:304–306. doi: 10.1016/0014-4827(72)90558-7. PubMed DOI
Endow S.A. Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics. 1982;100:375–385. PubMed PMC
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. 1991;19:4780. doi: 10.1093/nar/19.17.4780. PubMed DOI PMC
Rovatsos M.T., Marchal J.A., Romero-Fernández I., Fernández F.J., Giagia-Athanosopoulou E.B., Sánchez A. Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res. 2011;19:869–882. doi: 10.1007/s10577-011-9242-3. PubMed DOI
Shaffer H.B., Minx P., Warren D.E., Shedlock A.M., Thomson R.C., Valenzuela N., Abramyan J., Amemiya C.T., Badenhorst D., Biggar K.K., et al. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol. 2013;14:R28. doi: 10.1186/gb-2013-14-3-r28. PubMed DOI PMC
Tollis M., DeNardo D.F., Cornelius J.A., Dolby G.A., Edwards T., Henen B.T., Karl A.E., Murphy R.W., Kusumi K. The Agassiz’s desert tortoise genome provides a resource for the conservation of a threatened species. PLoS ONE. 2017;12:e0177708. doi: 10.1371/journal.pone.0177708. PubMed DOI PMC
Brian Simison W., Parham J.F., Papenfuss T.J., Lam A.W., Henderson J.B. An annotated chromosome-level reference genome of the Red-Eared Slider Turtle (Trachemys scripta elegans) Genome Biol. Evol. 2020;12:456–462. doi: 10.1093/gbe/evaa063. PubMed DOI PMC
Bickham J.W., Baker R.J. Chromosome homology and evolution of emydid turtles. Chromosoma. 1976;54:201–219. doi: 10.1007/BF00293451. PubMed DOI
De Smet W.H.O. The chromosomes of 11 species of Chelonia (Reptilia) Acta Zool. Pathol. Antverp. 1978;70:15–34.
Haiduk M.W., Bickham J.W. Chromosomal homologies and evolution of testudinoid turtles with emphasis on the systematic placement of Platysternon. Copeia. 1982;1982:60–66. doi: 10.2307/1444268. DOI
Scardino R., Mazzoleni S., Rovatsos M., Vecchioni L., Dumas F. Molecular cytogenetic characterization of the Sicilian endemic pond turtle Emys trinacris and the yellow-bellied slider Trachemys scripta scripta (Testudines, Emydidae) Genes. 2020;11:702. doi: 10.3390/genes11060702. PubMed DOI PMC
Nanda I., Schrama D., Feichtinger W., Haaf T., Schartl M., Schmid M. Distribution of telomeric (TTAGGG)(n) sequences in avian chromosomes. Chromosoma. 2002;111:215–227. doi: 10.1007/s00412-002-0206-4. PubMed 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
de Oliveira E.H., Habermann F.A., Lacerda O., Sbalqueiro I.J., Wienberg J., Müller S. Chromosome reshuffling in birds of prey: The karyotype of the world’s largest eagle (Harpy eagle, Harpia harpyja) compared to that of the chicken (Gallus gallus) Chromosoma. 2005;114:338–343. doi: 10.1007/s00412-005-0009-5. PubMed DOI
Galgon F., Fritz U. Captive bred hybrids between Chinemys reevesii (Gray, 1831) and Cuora amboinensis kamaroma Rummler & Fritz, 1991 (Testudines: Geoemydidae) Herpetozoa. 2002;15:137–148.
Wink M., Guicking D., Fritz U. Molecular evidence for hybrid origin of Mauremys iversoni Pritchard et McCord 1991, and Mauremys pritchardi McCord, 1997. Zool. Abh. Mus. Tierkd. Dresd. 2001;51:41–49.
Buskirk J.R., Parham J.F., Feldman C.R. On the hybridization between two distantly related Asian turtles (Testudines: Sacalia x Mauremys) Salamandra. 2005;41:21–26.
Schilde M., Barth D., Fritz U. An Ocadia sinensis x Cyclemys shanensis hybrid. Asian Herpetol. Res. 2004;10:120–125.
Stuart B.L., Parham J.F. Recent hybrid origin of three rare Chinese turtles. Conserv. Genet. 2007;8:169–175. doi: 10.1007/s10592-006-9159-0. DOI
Xia X., Wang L., Nie L., Huang Z., Jiang Y., Jing W., Liu L. Interspecific hybridization between Mauremys reevesii and Mauremys sinensis: Evidence from morphology and DNA sequence data. Afr. J. Biotechnol. 2011;10:6716–6724.
Suzuki D., Yabe T., Hikida T. Hybridization between Mauremys japonica and Mauremys reevesii inferred by nuclear and mitochondrial DNA analyses. J. Herpetol. 2013;48:445–454. doi: 10.1670/11-320. DOI