Revisiting the Karyotypes of Alligators and Caimans (Crocodylia, Alligatoridae) after a Half-Century Delay: Bridging the Gap in the Chromosomal Evolution of Reptiles

. 2021 Jun 05 ; 10 (6) : . [epub] 20210605

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34198806

Grantová podpora
2018/22033-1 Fundação de Amparo à Pesquisa do Estado de São Paulo
302449/2018-3 Conselho Nacional de Desenvolvimento Científico e Tecnológico

Although crocodilians have attracted enormous attention in other research fields, from the cytogenetic point of view, this group remains understudied. Here, we analyzed the karyotypes of eight species formally described from the Alligatoridae family using differential staining, fluorescence in situ hybridization with rDNA and repetitive motifs as a probe, whole chromosome painting (WCP), and comparative genome hybridization. All Caimaninae species have a diploid chromosome number (2n) 42 and karyotypes dominated by acrocentric chromosomes, in contrast to both species of Alligatorinae, which have 2n = 32 and karyotypes that are predominantly metacentric, suggesting fusion/fission rearrangements. Our WCP results supported this scenario by revealing the homeology of the largest metacentric pair present in both Alligator spp. with two smaller pairs of acrocentrics in Caimaninae species. The clusters of 18S rDNA were found on one chromosome pair in all species, except for Paleosuchus spp., which possessed three chromosome pairs bearing these sites. Similarly, comparative genomic hybridization demonstrated an advanced stage of sequence divergence among the caiman genomes, with Paleosuchus standing out as the most divergent. Thus, although Alligatoridae exhibited rather low species diversity and some level of karyotype stasis, their genomic content indicates that they are not as conserved as previously thought. These new data deepen the discussion of cytotaxonomy in this family.

Zobrazit více v PubMed

Grigg G., Seebacher F., Franklin C.E., editors. Crocodilian Biology and Evolution. 1st ed. Surrey Beatty; Chipping Norton, Australia: 2001. p. 446.

Brochu C.A. Phylogenetic approaches toward crocodylian history. Annu. Rev. Earth and Planet. Sci. 2003;31:357–397. doi: 10.1146/annurev.earth.31.100901.141308. DOI

Bronzati M., Montefeltro F.C., Langer M.C. Diversification events and the effects of mass extinction on Crocodyliformes evolutionary history. R. Soc. Open Sci. 2015;2:140385. doi: 10.1098/rsos.140385. PubMed DOI PMC

Stubbs T.L., Pierce S.E., Elsler A., Anderson P.S.L., Rayfield E.J., Benton M.J. Ecological opportunity and the rise and fall of crocodylomorph evolutionary innovation. Proc. R. Soc. B. 2021;288:20210069. doi: 10.1098/rspb.2021.0069. PubMed DOI PMC

Janke A., Arnason U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent Archosauria (birds and crocodiles) Mol. Biol. Evol. 1997;14:1266–1272. doi: 10.1093/oxfordjournals.molbev.a025736. PubMed DOI

Iwabe N., Hara Y., Kumazawa Y., Shibamoto K., Saito Y., Miyata T., Katoh K. Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol. Biol. Evol. 2005;22:810–813. doi: 10.1093/molbev/msi075. PubMed DOI

Green R.E., Braun E.L., Armstrong J., Earl D., Nguyen N., Hickey G., Vandewege M.W., St. John J.A., Capella-Gutiérrez S., Castoe T.A. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science. 2014;346:1254449. doi: 10.1126/science.1254449. PubMed DOI PMC

Pan T., Miao J.-S., Zhang H.-B., Yan P., Lee P.-S., Jiang X.-Y., Ouyang J.-H., Deng Y.-P., Zhang B.-W., Wu X.-B. Near-complete phylogeny of extant Crocodylia (Reptilia) using mitogenome-based data. Zool. J. Linn. Soc. 2021;191:1075–1089. doi: 10.1093/zoolinnean/zlaa074. DOI

Espinosa E., Godshalk R., Hall P., Thorbjarnarson J., Tucker A., Verdade L. Species Accounts. In: Ross P., editor. Status Survey and Conservation Action Plan: Revised Action Plan for Crocodiles. 2nd ed. Volume 1. IUCN/SSC Crocodile Specialist Group; Gland, Switzerland: Cambridge, UK: 1998. pp. 3–73.

Rueda-Almonacid J.V., Carr J.L., Mittermeier R.A., Rodríguez-Mahecha J.V., Mast R.B., Vogt R.C., Rhodin A.G.J., Ossa-Velásquez J.O., Rueda J.N., Mittermeier C.G. Orden Crocodylia. In: Mittermeier R.A., Rylands A., editors. Conservación Internacional. Serie de Guías Tropicales de Campo N° 6. Las Tortugas y lós Crocodilianos de los Países Andinos del Trópico. 1st ed. Volume 1. Editorial Panamericana, Formas e Impresos; Bogotá, Colombia: 2007. pp. 387–432.

Meredith R.W., Hekkala E.R., Amato G., Gatesy J. A phylogenetic hypothesis for Crocodylus (Crocodylia) based on mitochondrial DNA: Evidence for a trans-Atlantic voyage from Africa to the New World. Mol. Phylogenet. Evol. 2011;60:183–191. doi: 10.1016/j.ympev.2011.03.026. PubMed DOI

Oaks J.R. A time-calibrated species tree of Crocodylia reveals a recent radiation of the true crocodiles. Evolution. 2011;65:3285–3297. doi: 10.1111/j.1558-5646.2011.01373.x. PubMed DOI

McAliley L.R., Willis R.E., Ray D.A., White P.S., Brochu C.A., Densmore L.D. Are crocodiles really monophyletic?—Evidence for subdivisions from sequence and morphological data. Mol. Phylogenet. Evol. 2006;39:16–32. doi: 10.1016/j.ympev.2006.01.012. PubMed DOI

Martin S. Global diversity of crocodiles (Crocodilia, Reptilia) in freshwater. Hydrobiologia. 2008;595:587–591. doi: 10.1007/s10750-007-9030-4. DOI

Hekkala E., Shirley M.H., Amato G., Austin J.D., Charter S., Thorbjarnarson J., Vliet K.A., Houck M.L., Desalle R., Blum M.J. An ancient icon reveals new mysteries: Mummy DNA resurrects a cryptic species within the Nile crocodile. Mol. Ecol. 2011;20:4199–4215. doi: 10.1111/j.1365-294X.2011.05245.x. PubMed DOI

Shirley M.H., Vliet K.A., Carr A.N., Austin J.D. Rigorous approaches to species delimitation have significant implications for African crocodilian systematics and conservation. Proc. R. Soc. B. 2014;281:20132483. doi: 10.1098/rspb.2013.2483. PubMed DOI PMC

Srikulnath K., Thapana W., Muangmai N. Role of chromosome changes in Crocodylus evolution and diversity. Genom. Inform. 2015;13:102–111. doi: 10.5808/GI.2015.13.4.102. PubMed DOI PMC

Barreiros J.P. Crocodylia: Uma Longa História de Sucesso Evolutivo. 1st ed. Atlântida Revista de Cultura; Açores, Portugal: 2016. pp. 1–12.

Muniz F.L., Ximenes A.M., Bittencourt P.S., Hernández-Rangel S.M., Campos Z., Hrbek T., Farias I.P. Detecting population structure of Paleosuchus trigonatus (Alligatoridae: Caimaninae) through microsatellites markers developed by next generation sequencing. Mol. Biol. Rep. 2019;46:1–12. doi: 10.1007/s11033-019-04709-7. PubMed DOI

Uetz P., Freed P., Aguilar R., Hošek J., editors. The Reptile Database. [(accessed on 31 August 2020)]; Available online: http://www.reptile-database.org.

Nicolai M.P.J., Matzke N.J. Trait-based range expansion aided in the global radiation of Crocodylidae. Glob. Ecol. Biogeogr. 2019;28:1244–1258. doi: 10.1111/geb.12929. DOI

Shirley M.H., Carr A.N., Nestler J.H., Vliet K.A., Brochu C.A. Systematic revision of the living African slender-snouted crocodiles (Mecistops Gray, 1844) Zootaxa. 2018;4504:151–193. doi: 10.11646/zootaxa.4504.2.1. PubMed DOI

Bezuijen M.R., Shwedick B., Simpson B.K., Staniewicz A., Stuebing R. Tomistoma schlegelii. IUCN Red List Threat. Species. 2014;2014:E.T21981A2780499. doi: 10.2305/IUCN.UK.2014-1.RLTS.T21981A2780499.en. DOI

Lee M.S.Y., Yates A.M. Tip-dating and homoplasy: Reconciling the shallow molecular divergences of modern gharials with their long fossil record. Proc. R. Soc. B. 2018;285:20181071. doi: 10.1098/rspb.2018.1071. PubMed DOI PMC

Muniz F.L., Campos Z., Rangel S.M.H., Martínez J.G., Souza B.C., De Thoisy B., Botero-Arias R., Hrbek T., Farias I.P. Delimitation of evolutionary units in Cuvier´s dwarf caiman, Paleosuchus palpebrosus (Cuvier, 1807): Insights from conservation of a broadly distributes species. Conserv. Genet. 2018;19:599–610. doi: 10.1007/s10592-017-1035-6. DOI

Bittencourt P.S., Campos Z., Muniz F.L., Marioni B., Souza B.C., Da Silveira R., de Thoisy B., Hrbek T., Farias I.P. Evidence of cryptic lineages within a small South American crocodilian: The Schneider´s dwarf caiman Paleosuchus trigonatus (Alligatoridae: Caimaninae) PeerJ. 2019;7:e6580. doi: 10.7717/peerj.6580. PubMed DOI PMC

Balaguera-Reina S.A., Velasco A. Caiman crocodilus. IUCN Red List Threat. Species. 2019;2019:E.T46584A3009688. doi: 10.2305/IUCN.UK.2019-1.RLTS.T46584A3009688.en. DOI

Jiang H., Wu X. Alligator sinensis. IUCN Red List Threat. Species. 2018;2018 doi: 10.2305/IUCN.UK.2018-1.RLTS.T867A3146005.en. DOI

Thorbjarnarson J., Wang X., Ming S., He L., Ding Y., Wu Y., McMurry S.T. Wild populations of the Chinese alligator approach extinction. Biol. Conserv. 2002;103:93–102. doi: 10.1016/S0006-3207(01)00128-8. DOI

Olmo E. Trends in the evolution of reptilian chromosomes. Integr. Comp. Biol. 2008;48:486–493. doi: 10.1093/icb/icn049. PubMed DOI

Deakin J.E., Ezaz T. Understanding the evolution of reptile chromosomes through applications of combined cytogenetics and genomics approaches. Cytogenet. Genome Res. 2019;157:7–20. doi: 10.1159/000495974. 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

Ezaz T., Quinn A.E., Miura I., Sarre S.D., Georges A., Graves J.A.M. The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res. 2005;13:763–776. doi: 10.1007/s10577-005-1010-9. PubMed DOI

Ezaz T., Valenzuela N., Grützner F., Miura I., Georges A., Burke R.L., Graves J.A.M. An XX/XY sex michrocromosome 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

Kawai A., Nishida-Umehara C., Ishijima J., Tsuda Y., Ota H., Matsuda Y. Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet. Genome Res. 2007;117:92–102. doi: 10.1159/000103169. PubMed DOI

Martinez P.A., Ezaz T., Valenzuela N., Georges A., Graves J.A.M. 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

Badenhorst D., Stanyon R., Engstrom T., Valenzuela N. A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae. Chromosome Res. 2013;21:137–147. doi: 10.1007/s10577-013-9343-2. PubMed DOI

Koubová M., Pokorná M.J., Rovatsos M., Farkačová K., Altmanová M., Kratochvil L. Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae) are differentiated sex chromosomes indeed so evolutionary stable? Chromosome Res. 2014;22:441–452. doi: 10.1007/s10577-014-9430-z. PubMed DOI

Matsubara K., Gamble T., Matsuda Y., Zarkower D., Sarre S.D., Georges A., Graves J.A.M., Ezaz T. Non-homologous sex chromosomes in two geckos (Gekkonidae: Gekkota) with female heterogamety. Cytogenet. Genome Res. 2014;143:251–258. doi: 10.1159/000366172. PubMed DOI

Montiel E.E., Badenhorst D., Tamplin J., Burke R.L., Valenzuela N. Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma. 2016;126:105–113. doi: 10.1007/s00412-016-0576-7. PubMed DOI

Viana P.F., Ezaz T., Cioffi M.B., Almeida B.J., Feldberg E. Evolutionary Insights of the ZW Sex Chromosomes in Snakes: A New Chapter Added by the Amazonian Puffing Snakes of the Genus Spilotes. Genes. 2019;10:288. doi: 10.3390/genes10040288. PubMed DOI PMC

Viana P.F., Ezaz T., Cioffi M.B., Liehr T., Al-Rikabi A., Goll L.G., Rocha A.M., Feldberg E. Landscape of snake’ sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories. Sci. Rep. 2020;10:12499. doi: 10.1038/s41598-020-69349-5. PubMed DOI PMC

Cohen M.M., Clark H.F. The somatic chromosomes of five crocodilian species. Cytogenetics. 1967;6:193–203. doi: 10.1159/000129941. PubMed DOI

Cohen M.M., Gans C. The chromosomes of the Order Crocodilia. Cytogenetics. 1970;9:81–105. doi: 10.1159/000130080. PubMed DOI

King M., Honeycutt R., Contreras N. Chromosomal repatterning in crocodiles: C, G, and N-banding and the in situ hybridization of 18S and 26S rRNA cistrons. Genetica. 1986;70:191–201. doi: 10.1007/BF00122186. DOI

Lui J.F., Valencia E.F.T., Boer J.A. Karyotypic analysis and chromosome biometry of cell cultures of the yellow throated alligator (Caiman latirostris DAUDIN) Rev. Brasil. Genet. 1994;17:165–169.

Valleley E.M.A., Harrison C.J., Cook Y., Ferguson M.W.J., Sharpe P.T. The karyotype of Alligator mississippiensis, and chromosomal mapping of the ZFY/X homologue, Zfc. Chromosoma. 1994;103:502–507. doi: 10.1007/BF00337388. PubMed DOI

Kawagoshi T., Nishida C., Ota H., Kumazawa Y., Endo H., Matsuda Y. Molecular structures of centromeric heterochromatin and karyotypic evolution in the Siamese crocodile (Crocodylus siamensis) (Crocodylidae, Crocodylia) Chromosome Res. 2008;16:1119–1132. doi: 10.1007/s10577-008-1263-1. PubMed DOI

Uno Y., Nishida C., Tarui H., Ishishita S., Takagi C., Nishimura O., Ishijima J., Ota H., Kosaka A., Matsubara K., et al. Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS ONE. 2012;7:e53027. doi: 10.1371/journal.pone.0053027. PubMed DOI PMC

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

Oliveira V.C.S., Viana P.F., Gross M.C., Feldberg E., Da Silveira R., Cioffi M.B., Bertollo L.A.C., Schneider C.H. Looking for genetic effects of polluted anthropized environments on Caiman crocodilus crocodilus (Reptilia, Crocodylia): A comparative genotoxic and chromosomal analysis. Ecotoxicol. Environ. Saf. 2021;209:111835. doi: 10.1016/j.ecoenv.2020.111835. PubMed DOI

Olmo E., Signorino G.G. Chromorep: A Reptile Chromosomes Database. [(accessed on 24 August 2020)]; Available online: http://chromorep.univpm.it/?q=node/13.

Degrandi T.M., Gunski R.J., Garnero A.V., Oliveira E.H.C., Kretschmer R., Souza M.S., Barcellos S.A., Hass I. The distribution of 45S rDNA sites in bird suggests multiple evolutionary histories. Genet. Mol. Biol. 2020;43:e20180331. doi: 10.1590/1678-4685-gmb-2018-0331. PubMed DOI PMC

Amavet P., Markariani R., Fenocchio A. Comparative cytogenetic analysis of the South American alligators Caiman latirostris and Caiman yacare (Reptilia, Alligatoridae) from Argentina. Caryologia. 2003;56:489–493. doi: 10.1080/00087114.2003.10589361. DOI

Valenzuela N. Temperature dependent sex determination in reptiles. In: Deeming D.C., editor. Reptilian Incubation: Environment & Behaviour. 1st ed. Volume 1. Nottinghan University Press; Nottingham, UK: 2004. pp. 65–80.

González E.J., Martínez-López M., Morales-Garduza M.A., García-Morales R., Charruau P., Gallardo-Cruz J.A. The sex-determination pattern in crocodilians: A systematic review of three decades of research. J. Anim. Ecol. 2019;88:1417–1427. doi: 10.1111/1365-2656.13037. PubMed DOI

Viana P.F., Ribeiro L.B., Lima T., de Carvalho V.T., Vogt R.C., Gross M.C., Feldberg E. An optimized protocol for obtaining mitotic chromosomes from cultured reptilian lymphocytes. Nucleus. 2016;59:191–195. doi: 10.1007/s13237-016-0174-3. DOI

Johnson Pokorná M., Altmanová M., Rovatsos M., Velenský P., Vodička R., Rehák I., Kratochvíl L. First description of the karyotype and sex chromosomes in the Komodo dragon (Varanus komodoensis) Cytogenet. Genome Res. 2016;148:284–291. doi: 10.1159/000447340. 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

Schmid M. Chromosome banding in Amphibia. IV. Differentiation of GC and AT-rich regions in Anura. Chromosoma. 1980;77:83–103. doi: 10.1007/BF00292043. PubMed DOI

Cioffi M.B., Martins C., Bertollo L.A.C. Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish, Hoplias malabaricus. BMC Genet. 2009;10:34. doi: 10.1186/1471-2156-10-34. PubMed DOI 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

Kubat Z., Hobza R., Vyskot B., Kejnovsky E. Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome. 2008;51:350–356. doi: 10.1139/G08-024. PubMed DOI

Yano C.F., Bertollo L.A.C., Cioffi M.B. Fish-FISH: Molecular Cytogenetics in Fish Species. In: Liehr T., editor. Fluorescence In Situ Hybridization (FISH)—Application Guide. 2nd ed. Volume 1. Springer; Berlin, Germany: 2017. pp. 429–444. DOI

Kosyakova N., Liehr T., Al-Rikabi A. FISH-microdissection. In: Liehr T., editor. Fluorescence In Situ Hybridization (FISH)—Application Guide. 2nd ed. Volume 1. Springer; Berlin, Germany: 2017. pp. 81–99. DOI

Sambrook J., Russell D.W. Molecular Cloning, A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press; New York, NY, USA: 2001. pp. 58–63.

Zwick M.S., Hanson R.E., McKnight T.D., Islam-Faridi M.N., Stelly D.M., Wing R.A., Price H.J. A rapid procedure for the isolation of C0t-1 DNA from plants. Genome. 1997;40:138–142. doi: 10.1139/g97-020. PubMed DOI

Symonová R., Sember A., Majtánová Z., Ráb P. Characterization of fish genomes by GISH and CGH. In: Ozouf-Costaz C., Pisano E., Foresti F., Toledo L.F.A., editors. Fish Cytogenetic Techniques Ray-Fin Fishes Chondrichthyans. 1st ed. CCR Press; Boca Raton, FL, USA: 2015. pp. 118–131.

Levan A., Fredga K., Sandberg A.A. Nomenclature for centromeric position on chromosomes. Hereditas. 1964;52:201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x. DOI

Matthey R., van Brink J.M. Sex chromosomes in Amniota. Evolution. 1957;11:163–165. doi: 10.1111/j.1558-5646.1957.tb02885.x. DOI

Ohno S. Sex Chromosomes and Sex-linked Genes. In: Labhart A., Mann T., Samuels L.T., Zander J., editors. Monographs on Endocrinology. 1st ed. Volume 1. Springer; Berlin, Germany: New York, NY, USA: 1967. pp. 33–46. DOI

Beçak W., Beçak M.L. Order: CROCODILIA, Suborder: EUSUCHIA, Family: CROCODYLIDAE, Caiman crocodilus (Linnaeus) Folio R-15. 1971;1:1–3.

Olmo E.A. Reptilia. In: John B., editor. Animal Cytogenetics. Chordata 3. 1st ed. Volume 4. Gebrueder Borntraeger; Berlin, Germany: Stuttgart, Germany: 1986. pp. 1–100.

Amavet P., Siroski P., Donayo P., Medina M. Karyotype of Caiman latirostris and Caiman yacare (Reptilia, Alligatoridae); Proceedings of the 15th Working Meeting of the Crocodile Specialist Group; Varadero, Cuba. 17–20 January 2000; pp. 135–138.

Alfaro M.E., Santini F., Brock C., Alamillo H., Dornburg A., Rabosky D.L., Carnevale G., Harmon L.J. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl. Acad. Sci. USA. 2009;106:13410–13414. doi: 10.1073/pnas.0811087106. PubMed DOI PMC

Jetz W., Thomas G.H., Joy J.B., Hartmann K., Mooers A.O. The global diversity of birds in space and time. Nature. 2012;491:444–448. doi: 10.1038/nature11631. PubMed DOI

Pyron R.A., Burbrink F.T., Wiens J.J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 2013;13:93. doi: 10.1186/1471-2148-13-93. PubMed DOI PMC

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

Rovatsos M., Altmanová M., Johnson Pokorná M., Velenský P., Baca A.S., Kratochvíl L. Evolution of karyotypes in chameleons. Genes. 2017;8:382. doi: 10.3390/genes8120382. PubMed DOI PMC

Müller J., Reisz R.R. Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. BioEssays. 2005;27:1069–1075. doi: 10.1002/bies.20286. PubMed DOI

Slijepcevic P. Telomere length and telomere-centromere relationships? Mutat. Res. 1998;404:215–220. doi: 10.1016/S0027-5107(98)00116-X. PubMed DOI

Porter C.A., Haiduk M.W., de Queiroz K. Evolution and phylogenetic significance of ribosomal gene location in chromosomes of squamate reptiles. Copeia. 1994;1994:302–313. doi: 10.2307/1446980. DOI

Sochorová J., Garcia S., Gálvez F., Symonová R., Kovařík A. Evolutionary trends in animal ribosomal DNA loci: Introduction to a new online database. Chromosoma. 2018;127:141–150. doi: 10.1007/s00412-017-0651-8. PubMed DOI PMC

Camper J.D., Hanks B. Variation in the nucleolus organizer region among new world snakes. J. Herpetol. 1995;29:468–471. doi: 10.2307/1565003. DOI

O’Meally S., Patel H.R., Stiglec R., Sarre S.D., Georges A., Graves J.A.M., Ezaz T. Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res. 2010;18:787–800. doi: 10.1007/s10577-010-9152-9. 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;10:4276. doi: 10.1038/s41598-020-61116-w. PubMed DOI PMC

Perry B.W., Schield D.R., Adams R.H., Castoe T.A. Microchromosomes exhibit distinct features of vertebrate chromosome structure and function with underappreciated ramifications for genome evolution. Mol. Biol. Evol. 2021;38:904–910. doi: 10.1093/molbev/msaa253. PubMed DOI PMC

Burt D.W. Origin and evolution of avian microchromosomes. Cytogenet. Genome Res. 2002;96:97–112. doi: 10.1159/000063018. PubMed DOI

Norris T.B., Rickards G.K., Daugherty C.H. Chromosomes of tuatara, Sphenodon, a chromosome heteromorphism and an archaic reptilian karyotype. Cytogenet. Genome Res. 2004;105:93–99. doi: 10.1159/000078014. PubMed DOI

Auer H., Mayr B., Lambrou M., Schleger W. An extended chicken karyotype, including the NOR chromosome. Cytogenet. Cell Genet. 1987;45:218–221. doi: 10.1159/000132457. PubMed DOI

McQueen H.A., Siriaco G., Bird A.P. Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res. 1998;8:621–630. doi: 10.1101/gr.8.6.621. PubMed DOI PMC

Smith J., Bruley C.K., Paton I.R., Dunn I., Jones C.T., Windsor D., Morrice D.R., Law A.S., Masabanda J., Sazanov A., et al. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim. Genet. 2000;31:96–103. doi: 10.1046/j.1365-2052.2000.00565.x. PubMed DOI

Andreozzi L., Federico C., Motta S., Saccone S., Sazanova A.L., Sazanov A.A., Smirnov A.F., Galkina S.A., Lukina N.A., Rodionov A.V., et al. Compositional mapping of chicken chromosomes and identification of the gene-richest regions. Chromosome Res. 2001;9:521–532. doi: 10.1023/A:1012436900788. PubMed DOI

Kuraku S., Ishijima J., Nishida-Umehara C., Agata K., Kuratani S., Matsuda Y. cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids. Chromosome Res. 2006;14:187–202. doi: 10.1007/s10577-006-1035-8. PubMed DOI

Olmo E. Rate of chromosome changes and speciation in reptiles. Genetica. 2005;125:185–203. doi: 10.1007/s10709-005-8008-2. PubMed DOI

Shedlock A.M., Botka C.W., Zhao S., Shetty J., Zhang T., Liu J.S., Deschavanne P.J., Edwards S.V. Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genome. Proc. Natl. Acad. Sci. USA. 2007;104:2767–2772. doi: 10.1073/pnas.0606204104. PubMed DOI PMC

Alföldi J., Di Palma F., Grabherr M., Williams C., Kong L., Mauceli E., Russell P., Lowe C.B., Glor R.E., Jaffe J.D., et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477:587–591. doi: 10.1038/nature10390. PubMed DOI PMC

Adams R.H., Blackmon H., Reyes-Velasco J., Schield D.R., Card D.C., Andrew A.L., Waynewood N., Castoe T.A. Microsatellite landscape evolutionary dynamics across 450 million years of vertebrate genome evolution. Genome. 2016;59:295–310. doi: 10.1139/gen-2015-0124. PubMed DOI

Kapusta A., Suh A., Feschotte C. Dynamics of genome size evolution in birds and mammals. Proc. Natl. Acad. Sci. USA. 2017;114:1–10. doi: 10.1073/pnas.1616702114. PubMed DOI PMC

Balaresque P., King T.E., Parkin E.J., Heyer E., Carvalho-Silva D., Kraaijenbrink T., de Knijff P., Tyler-Smith C., Jobling M.A. Gene conversion violates the stepwise mutation model for microsatellites in Y-chromosomal palindromic repeats. Hum. Mutat. 2014;35:609–617. doi: 10.1002/humu.22542. PubMed DOI PMC

Ramsay L., Macaulay M., Cardle L., Morgante M., Ivanissevich S.d., Maestri E., Powell W., Waugh R. Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant. J. 1999;17:415–425. doi: 10.1046/j.1365-313X.1999.00392.x. PubMed DOI

Cordaux R., Batzer M.A. The impact of retrotransposon on human genome evolution. Nat. Rev. Genet. 2009;10:691–703. doi: 10.1038/nrg2640. PubMed DOI PMC

Janes D.E., Organ C.L., Fujita M.K., Shedlock A.M., Edwards S.V. Genome evolution in reptilia, the sister group of mammals. Annu. Rev. Genom. Hum. Genet. 2010;11:239–264. doi: 10.1146/annurev-genom-082509-141646. PubMed DOI

Figliuolo V.S.P., Goll L., Viana P.F., Feldberg E., Gross M.C. First record on sex chromosomes in a species of the family Cynodontidae: Cynodon gibbus (Agassiz, 1829) Cytogenet Genome Res. 2020;160:29–37. doi: 10.1159/000505889. PubMed DOI

Pasquesi G.I.M., Adams R.H., Card D.C., Schield D.R., Corbin A.B., Perry B.W., Reyes-Velasco J., Ruggiero R.P., Vandewege M.W., Shortt J.A., et al. Squamate reptiles challenge paradigms of genomic repeat element evolution set by birds and mammals. Nat. Commun. 2018;9:2774. doi: 10.1038/s41467-018-05279-1. PubMed DOI PMC

Ahmad S.F., Singchat W., Jehangir M., Suntronpong A., Panthum T., Malaivijitnond M., Srikulnath K. Dark matter of primate genomes: Satellite DNA repeats and their evolutionary dynamics. Cells. 2020;9:2714. doi: 10.3390/cells9122714. PubMed DOI PMC

Lim K.Y., Kovarik A., Matyasek R., Chase M.W., Clarkson J.J., Grandbastien M.A., Leitch A.R. Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 2007;175:756–763. doi: 10.1111/j.1469-8137.2007.02121.x. PubMed DOI

Majka J., Majka M., Kwiatek M., Wiśniewska H. Similarities and differences in the nuclear genome organization within Pooideae species revealed by comparative genomic in situ hybridization (GISH) J. Appl. Genet. 2017;58:151–161. doi: 10.1007/s13353-016-0369-y. PubMed DOI PMC

Barby F.F., Bertollo L.A.C., de Oliveira E.A., Yano C.F., Hatanaka T., Ráb P., Sember A., Ezaz T., Artoni R.F., Liehr T., et al. Emerging patterns of genome organization in Notopteridae species (Teleostei, Osteoglossiformes) as revealed by Zoo-FISH and Comparative Genomic Hybridization (CGH) Sci. Rep. 2019;9:1112. doi: 10.1038/s41598-019-38617-4. PubMed DOI PMC

Matsuoka M.P., Gharrett A.J., Wilmot R.L., Smoker W.W. Genetic linkage mapping of allozyme loci in even- and odd-year pink salmon (Oncorhynchus gorbuscha) J. Hered. 2004;95:421–429. doi: 10.1093/jhered/esh069. PubMed DOI

Mandáková T., Joly S., Krzywinski M., Mummenhoff K., Lysak M.A. Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant. Cell. 2010;22:2277–2290. doi: 10.1105/tpc.110.074526. PubMed DOI PMC

Bomfleur B., Decombeix A.-L., Schwendemann A.B., Escapa I.H., Taylor E.L., Taylor T.N., McLoughlin S. Habit and ecology of the petriellales, an unusual group of seed plants from the Triassic of Gondwana. Int. J. Plant. Sci. 2014;175:1062–1075. doi: 10.1086/678087. DOI

Samad M.S., Biswas A., Bakken L.R., Clough T.J., de Klein C.A.M., Richards K.G., Lanigan G.J., Morales S.E. Phylogenetic and functional potential links pH and N2O emission in pasture soils. Sci Rep. 2016;6:35990. doi: 10.1038/srep35990. PubMed DOI PMC

Sessions S.K., Kezer J. Evolutionary cytogenetics of Bolitoglossine salamanders (Family Plethodontidae) In: Green D.M., Sessions S.K., editors. Amphibian Cytogenetics and Evolution. 1st ed. San Diego Academic Press; San Diego, CA, USA: 1991. pp. 89–130. DOI

Aprea G., Andreone G., Capriglione T., Odierna V., Vences M. Evidence for a remarkable stasis of chromosome evolution in Malagasy tree-frogs (Boophis: Mantellidae) Ital. J. Zool. 2004;2:237–243. doi: 10.1080/11250000409356641. DOI

Ellegren H. Evolutionary stasis: The stable chromosome of birds. Trends Ecol. Evol. 2010;25:283–291. doi: 10.1016/j.tree.2009.12.004. PubMed DOI

Molina W.F. Chromosomal changes and stasis in marine fish groups. In: Pisano E., Ozouf-Costaz C., Foresti F., Kapoor B.G., editors. Fish Cytogenetics. 1st ed. CRC Press; Boca Raton, FL, USA: 2007. pp. 69–110. DOI

Gaffaroglu M., Majtánová Z., Symonová R., Pelikánová S., Unal S., Lajbner Z., Ráb P. Present and future salmonid cytogenetics. Genes. 2020;11:1462. doi: 10.3390/genes11121462. PubMed DOI PMC

Barby F.F., Ráb P., Lavoué S., Ezaz T., Bertollo L.A.C., Kilian A., Maruyama S.R., de Oliveira E.A., Artoni R.A., Santos M.H. From chromosomes to genome: Insights into the evolutionary relationships and biogeography of Old World knifefishes (Notopteridae; Osteoglossiformes) Genes. 2018;9:306. doi: 10.3390/genes9060306. PubMed DOI PMC

Wake D.B., Roth G., Wake M.H. On the problem of stasis in organismal evolution. J. Theor. Biol. 1983;101:211–224. doi: 10.1016/0022-5193(83)90335-1. DOI

Stockdale M.T., Benton M.J. Environmental drivers of body size evolution in crocodile-line archosaurs. Commun. Biol. 2021;4:38. doi: 10.1038/s42003-020-01561-5. PubMed DOI PMC

White M.J.D. Animal Cytology and Evolution. 3rd ed. Cambridge University Press; Cambridge, UK: 1973. p. 468.

King M. Chromosome change and speciation in lizards. In: Atchley W.R., Woodruff D.S., editors. Essays on Evolution and Speciation in Honour of M. J. D. 1st ed. Cambridge University Press; London, UK: 1981. pp. 262–285.

White M.J.D. Modes of Speciation. 1st ed. W.R. Freeman and Company; San Francisco, CA, USA: 1978.

King M. Species Evolution: The Role of Chromosome Change. 3rd ed. Cambridge University Press; Cambridge, UK: 1995. p. 322.

Potter S., Bragg J.G., Blom M.P.K., Deakin J.E., Kirkpatrick M., Eldridge M.D.B., Moritz C. Chromosomal speciation in the genomics era: Disentangling phylogenetic evolution of rock-wallabies. Front. Genet. 2017;8:10. doi: 10.3389/fgene.2017.00010. PubMed DOI PMC

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