Matamatas Chelus spp. (Testudines, Chelidae) have a remarkable evolutionary history of sex chromosomes with a long-term stable XY microchromosome system.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
23 04 2022
23 04 2022
Historique:
received:
15
02
2022
accepted:
11
04
2022
entrez:
24
4
2022
pubmed:
25
4
2022
medline:
27
4
2022
Statut:
epublish
Résumé
The genus Chelus, commonly known as Matamata is one of the most emblematic and remarkable species among the Neotropical chelids. It is an Amazonian species with an extensive distribution throughout Negro/Orinoco and Amazonas River basins. Currently, two species are formally recognized: Chelus orinocensis and Chelus fimbriata and although it is still classified as "Least Concern" in the IUCN, the Matamatas are very appreciated and illegally sold in the international pet trade. Regardless, little is known regarding many aspects of its natural history. Chromosomal features for Chelus, for instance, are meagre and practically restricted to the description of the diploid number (2n = 50) for Chelus fimbriata, and its sex determining strategies are yet to be fully investigated. Here, we examined the karyotype of Chelus fimbriata and the newly described Chelus orinocensis, applying an extensive conventional and molecular cytogenetic approach. This allowed us to identify a genetic sex determining mechanism with a micro XY sex chromosome system in both species, a system that was likely present in their most common recent ancestor Chelus colombiana. Furthermore, the XY system found in Chelus orinocensis and Chelus fimbriata, as seen in other chelid species, recruited several repeat motifs, possibly prior to the split of South America and Australasian lineages, indicating that such system indeed dates back to the earliest lineages of Chelid species.
Identifiants
pubmed: 35461353
doi: 10.1038/s41598-022-10782-z
pii: 10.1038/s41598-022-10782-z
pmc: PMC9035145
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6676Informations de copyright
© 2022. The Author(s).
Références
Ferreira, G. S. & Langer, M. C. A pelomedusoid (Testudines, Pleurodira) plastron from the Lower Cretaceous of Alagoas, Brazil. Cretaceous Res. 46, 267–271 (2013).
doi: 10.1016/j.cretres.2013.10.001
Romano, P. S. R., Gallo, V., Ramos, R. R. C. & Antonioli, L. Atolchelys lepida, a new side-necked turtle from the Early Cretaceous of Brazil and the age of crown Pleurodira. Biol. Lett. 10, 1–10 (2014).
doi: 10.1098/rsbl.2014.0290
Ferreira, G. S., Bronzati, M., Langer, M. C. & Sterli, J. Phylogeny, biogeography and diversification patterns of side-necked turtles (Testudines: Pleurodira). R. Soc. Open Sci. 5, 1–17 (2018).
doi: 10.1098/rsos.171773
de la Fuente, M. S., Umazano, A. M., Sterli, J. & Carballido, J. L. New chelid turtles of the lower section of the Cerro Barcino formation (Aptian-Albian?), Patagonia, Argentina. Cretaceous Res. 32, 527–537 (2011).
doi: 10.1016/j.cretres.2011.03.007
Joyce, W. G., Parham, J. F., Lyson, T. R., Warnock, R. C. M. & Donoghue, P. C. J. A divergence dating analysis of turtles using fossil calibrations: An example of best practices. J. Paleontol. 87, 612–634 (2013).
doi: 10.1666/12-149
Pereira, A. G., Sterli, J., Moreira, F. R. R. & Schrago, C. G. Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Mol. Phylogenet. Evol. 113, 59–66 (2017).
pubmed: 28501611
doi: 10.1016/j.ympev.2017.05.008
Shaffer, H. B., McCartney-Melstad, E., Near, T. J., Mount, G. G. & Spinks, P. Q. Phylogenomic analyses of 539 highly informative loci dates a fully resolved time tree for the major clades of living turtles (Testudines). Mol. Phylogenet. Evol. 115, 7–15 (2017).
pubmed: 28711671
doi: 10.1016/j.ympev.2017.07.006
Rueda-Almonacid, J. Vicente. Las tortugas y los cocodrilianos de los países andinos de trópico (Conservación Internacional, 2007).
Georges, A. & Thomson, S. Diversity of Australasian freshwater turtles, with an annotated synonymy and keys to species. Zootaxa 2496, 1–37 (2010).
doi: 10.11646/zootaxa.2496.1.1
TTWG. Turtles of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status, 9th ed. Vol. 8 (Chelonian Research Foundation and Turtle Conservancy, 2021).
Uetz, P., F. P. A. R. & H. J. The Reptile Database. http://www.reptile-database.org/ (2022).
Antonelli, A. et al. Amazonia is the primary source of Neotropical biodiversity. Proc. Natl. Acad. Sci. U.S.A. 115, 6034–6039 (2018).
pubmed: 29760058
pmcid: 6003360
doi: 10.1073/pnas.1713819115
Mittermeier, R. A., van Dijk, P. P., Rhodin, A. G. J. & Nash, S. D. Turtle hotspots: An analysis of the occurrence of tortoises and freshwater turtles in biodiversity hotspots, high-biodiversity wilderness areas, and turtle priority areas. Chelonian Conserv. Biol. 14, 2–10 (2015).
doi: 10.2744/ccab-14-01-2-10.1
Cunha, F. A. G., Sampaio, I., Carneiro, J. & Vogt, R. C. A New Species of Amazon Freshwater Toad-Headed Turtle in the Genus Mesoclemmys (Testudines: Pleurodira: Chelidae) from Brazil. Chelonian Conserv. Biol. 20, 151–166 (2021).
doi: 10.2744/CCB-1448.1
Brito, E. S. et al. New records of mesoclemmys raniceps (Testudines, chelidae) for the states of amazonas, pará and Rondônia, north Brazil, including the Tocantins basin. Herpetol. Notes 12, 283–289 (2019).
Cunha, F. A. G. et al. Distribution of Chelus fimbriata and Chelus orinocensis (Testudines: Chelidae). Chelonian Conserv. Biol. 20, 109–115 (2021).
doi: 10.2744/CCB-1398.1
Pritchard, P. Chelus fimbriata (Schneider 1783)—Matamata Turtle. In Conservation Biology of Freshwater Turtles and Tortoises 020.1–020.10 (Chelonian Research Foundation, 2008). https://doi.org/10.3854/crm.5.020.fimbriata.v1.2008 .
Vogt, R. C. Tartarugas da Amazônia (2008).
Holmstrom, W. F. Preliminary observations on prey herding in the Matamata turtle, Chelus fimbriatus (Reptilia, Testudines, Chelidae). J. Herpetol. 12, 573 (1978).
doi: 10.2307/1563365
Teran, A. F., Vogt, R. C. & de Fatima Soares Gomez, M. Food Habits of an assemblage of five species of turtles in the Rio Guapore, Rondonia, Brazil. J. Herpetol. 29, 536 (1995).
doi: 10.2307/1564736
Vargas-Ramírez, M. et al. Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography. Mol. Phylogenet. Evol. 148 (2020).
Lasso, C. A. et al. Conservación y tráfico de la tortuga matamata, Chelus fimbriata (Schneider, 1783) en Colombia: un ejemplo del trabajo conjunto entre el Sistema Nacional Ambiental, ONG y academia. Biota Colombiana 19, 147–159 (2018).
doi: 10.21068/c2018.v19n01a10
Barros, R. M., Sampaio, M. M., Assis, M. F., Ayres, M. & Cunha, O. R. General considerations on the karyotypic evolution of chelonia from the Amazon Region of Brazil. Cytologia 41, 559–565 (1976).
doi: 10.1508/cytologia.41.559
Bull, J. J. & Legler, J. M. Karyotypes of side-necked turtles (Testudines: Pleurodira). Can. J. Zool. 58, 828–841 (1980).
Viana, P. F. et al. An optimized protocol for obtaining mitotic chromosomes from cultured reptilian lymphocytes. Nucleus 59,1–5 (2016).
Mcbee, K., Bickham, J. W., Rhodin, A. G. J. & Mittermeier, R. A. Karyotypic Variation in the Genus Platemys (Testudines: Pleurodira). Copeia 2, 445–449 (1987).
Mazzoleni, S. et al. Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae). Scientific Reports 10, 1–11 (2020).
Viana, P. F. et al. 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 9, 1–15 (2020).
Ewert, M. A., Etcheberger, C. R. & Nelson, C. E. Turtle Sex-determining modes and TSD Patterns, and Some TSD Pattern Correlates 21–32 (Smithsonian Books, Washington, 2004).
Ferreira-Júnior Paulo. Aspectos Ecológicos da Determinação Sexual em Tartarugas. 39, 139–154 (2009).
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. Chromosom. Res. 16, 815–825 (2008).
doi: 10.1007/s10577-008-1228-4
Lee, L. S., Montiel, E. E. & Valenzuela, N. Discovery of putative XX/XY male heterogamety in emydura subglobosa turtles exposes a novel trajectory of sex chromosome evolution in emydura. Cytogenet. Genome Res. 158, 160–169 (2019).
pubmed: 31394537
doi: 10.1159/000501891
Ezaz, T. et al. An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosom. Res. 14, 139–150 (2006).
doi: 10.1007/s10577-006-1029-6
van Doorn, G. S. Evolutionary transitions between sex-determining mechanisms: A review of theory. Sex. Dev. 8, 7–19 (2014).
pubmed: 24335102
doi: 10.1159/000357023
van Doorn, G. S. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007).
pubmed: 17943130
doi: 10.1038/nature06178
Beukeboom, L. W. & Perrin, N. The Evolution of Sex Determination (Oxford University Press, Oxford, 2014).
doi: 10.1093/acprof:oso/9780199657148.001.0001
Bachtrog, D. et al. Sex determination: Why so many ways of doing it?. PLoS Biology 12, e1001899 (2014).
pubmed: 24983465
pmcid: 4077654
doi: 10.1371/journal.pbio.1001899
Viana, P. F. et al. Landscape of snake’ sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories. Sci. Rep. 10, 1–14 (2020).
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. 32, 1296–1309 (2015).
pubmed: 25657328
doi: 10.1093/molbev/msv023
Pennell, M. W., Mank, J. E. & Peichel, C. L. Transitions in sex determination and sex chromosomes across vertebrate species. Mol. Ecol. 27, 3950–3963 (2018).
pubmed: 29451715
pmcid: 6095824
doi: 10.1111/mec.14540
Valenzuela, N. & Adams, D. C. Chromosome number and sex determination coevolve in turtles. Evolution 65, 1808–1813 (2011).
pubmed: 21644965
doi: 10.1111/j.1558-5646.2011.01258.x
Sabath, N. et al. Sex determination, longevity, and the birth and death of reptilian species. Ecol. Evol. 6, 5207–5220 (2016).
pubmed: 27551377
pmcid: 4984498
doi: 10.1002/ece3.2277
Literman, R., Burrett, A., Bista, B. & Valenzuela, N. Putative independent evolutionary reversals from genotypic to temperature-dependent sex determination are associated with accelerated evolution of sex-determining genes in turtles. J. Mol. Evol. 86, 11–26 (2018).
pubmed: 29192334
doi: 10.1007/s00239-017-9820-x
Bista, B., Wu, Z., Literman, R. & Valenzuela, N. Thermosensitive sex chromosome dosage compensation in ZZ/ZW softshell turtles, Apalone spinifera. Philos. Trans. R. Soc. B Biol. Sci. 376, 1–14 (2021).
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 126, 105–113 (2017).
pubmed: 26842819
doi: 10.1007/s00412-016-0576-7
Lee, L., Montiel, E. E., Navarro-Domínguez, B. M. & Valenzuela, N. Chromosomal rearrangements during turtle evolution altered the synteny of genes involved in vertebrate sex determination. Cytogenet. Genome Res. 157, 77–88 (2019).
pubmed: 30808820
doi: 10.1159/000497302
Bista, B. & Valenzuela, N. Turtle insights into the evolution of the reptilian karyotype and the genomic architecture of sex determination. Genes 11, 1–11 (2020).
Zexian, Z. et al. Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing. bioRxiv (2021).
Cunha, F. A. G., Fernandes, T., Franco, J. & Vogt, R. C. Reproductive biology and hatchling morphology of the amazon toad-headed turtle (Mesoclemmys raniceps) (Testudines: Chelidae), with notes on species morphology and taxonomy of the mesoclemmys group. Chelonian Conserv. Biol. 18, 195 (2019).
doi: 10.2744/CCB-1271.1
Matsubara, K. et al. Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida. Chromosoma 125, 111–123 (2016).
pubmed: 26194100
doi: 10.1007/s00412-015-0531-z
Gorman, G. C. The chromosomes of Reptilia, a cytotaxonomic interpretation. In Cytotaxonomy and Vertebrate Evolution 347–424 (1973).
Reed, K. M. et al. Cytogenetic analysis of the pleurodine turtle Phrynops hogei and its taxonomic implications. Amphibia Reptilia 12, 203–212 (1991).
doi: 10.1163/156853891X00176
Cavalcante, M. G. et al. Physical mapping of repetitive DNA suggests 2n reduction in Amazon turtles Podocnemis (Testudines: Podocnemididae). PLoS ONE 13, 1–13 (2018).
doi: 10.1371/journal.pone.0197536
Clemente, L. et al. Interstitial telomeric repeats are rare in turtles. Genes 11, 1–18 (2020).
doi: 10.3390/genes11060657
Singchat, W. et al. Chromosome map of the Siamese cobra: Did partial synteny of sex chromosomes in the amniote represent “a hypothetical ancestral super-sex chromosome” or random distribution?. BMC Genomics 19, 1–16 (2018).
doi: 10.1186/s12864-018-5293-6
Srikulnath, K., Azad, B., Singchat, W. & Ezaz, T. Distribution and amplification of interstitial telomeric sequences (ITSs) in Australian dragon lizards support frequent chromosome fusions in Iguania. PLoS ONE 14, 1–11 (2019).
doi: 10.1371/journal.pone.0212683
Abramyan, J., Ezaz, T., Graves, J. A. M. & Koopman, P. Z and W sex chromosomes in the cane toad (Bufo marinus). Chromosom. Res. 17, 1015–1024 (2009).
doi: 10.1007/s10577-009-9095-1
Born, G. G. & Bertollo, L. A. C. An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing × chromosome. Chromosom. Res. 8, 111–118 (2000).
doi: 10.1023/A:1009238402051
O’Meally, D. et al. Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosom. Res. 18, 787–800 (2010).
doi: 10.1007/s10577-010-9152-9
Ferreira, M., Garcia, C., Matoso, D. A., de Jesus, I. S. & Feldberg, E. A new multiple sex chromosome system X1X1X2X2/X1Y1X2Y2 in siluriformes: Cytogenetic characterization of Bunocephalus coracoideus (Aspredinidae). Genetica 144, 591–599 (2016).
pubmed: 27687472
doi: 10.1007/s10709-016-9927-9
Yano, C. F., Bertollo, L. A. C., Liehr, T., Troy, W. P. & de Cioffi, M. B. W. Chromosome dynamics in Triportheus Species (Characiformes, Triportheidae): An ongoing process narrated by repetitive sequences. J. Hered. 107, 342–348 (2016).
pubmed: 27036509
pmcid: 4888443
doi: 10.1093/jhered/esw021
Symonová, R. Integrative rDNAomics-importance of the oldest repetitive fraction of the eukaryote genome. Genes 10, 1–14 (2019).
doi: 10.3390/genes10050345
Kawai, A. et al. Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet. Genome Res. 117, 92–102 (2007).
pubmed: 17675849
doi: 10.1159/000103169
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. Chromosom. Res. 21, 137–147 (2013).
doi: 10.1007/s10577-013-9343-2
Viana, P. F. et al. Genomic organization of repetitive DNAs and differentiation of an XX/XY sex chromosome system in the Amazonian Puffer Fish, Colomesus asellus (Tetraodontiformes). Cytogen. Genome Research 153, 1–9 (2018).
Castoe, T. A. et al. Discovery of highly divergent repeat landscapes in snake genomes using high-throughput sequencing. Genome Biol. Evol. 3, 641–653 (2011).
pubmed: 21572095
pmcid: 3157835
doi: 10.1093/gbe/evr043
Castoe, T. A. et al. Sequencing the genome of the Burmese python (Python molurus bivittatus) as a model for studying extreme adaptations in snakes. Genome Biol. 12, 1–8 (2011).
doi: 10.1186/gb-2011-12-7-406
Card, D. C. et al. Two low coverage bird genomes and a comparison of reference-guided versus de novo genome assemblies. PLoS ONE 9, e106649 (2014).
pubmed: 25192061
pmcid: 4156343
doi: 10.1371/journal.pone.0106649
Adams, R. H. et al. Microsatellite landscape evolutionary dynamics across 450 million years of vertebrate genome evolution. Genome 59, 295–310 (2016).
pubmed: 27064176
doi: 10.1139/gen-2015-0124
Pearson, C. E. & Sinden, R. R. Alternative structures in duplex DNA formed within the trinucleotide repeats of the myotonic dystrophy and fragile × loci. Biochemistry 35, 5041–5053 (1996).
pubmed: 8664297
doi: 10.1021/bi9601013
Chamberlain, N. L., Driver, E. D. & Miesfeld, R. L. The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res. 22, 3181–3186 (1994).
pubmed: 8065934
pmcid: 310294
doi: 10.1093/nar/22.15.3181
Sandberg, G. Effect of in vitro promoter methylation and CGG repeat expansion on FMR-1 expression. Nucleic Acids Res. 25, 2883–2887 (1997).
pubmed: 9207038
pmcid: 146834
doi: 10.1093/nar/25.14.2883
Rubinsztein, D. C. et al. Microsatellite evolution—evidence for directionality and variation in rate between species. Nat. Genet. 10, 337–343 (1995).
pubmed: 7670473
doi: 10.1038/ng0795-337
Eisen, J. A. Mechanistic basis for microsatellite instability. In Microsatellites: Evolution and Applications (eds Goldstein, D. B. & Schlotterer, C.) 34–48 (Oxford University Press, Oxford, 1999).
Payseur, B. A. & Nachman, M. W. Microsatellite variation and recombination rate in the human genome. Genetics 156, 1285–1298 (2000).
pubmed: 11063702
pmcid: 1461344
doi: 10.1093/genetics/156.3.1285
Li, Y. C., Korol, A. B., Fahima, T., Beiles, A. & Nevo, E. Microsatellites: Genomic distribution, putative functions and mutational mechanisms: A review. Molecular ecology 11, 2453–2465 (2002).
pubmed: 12453231
doi: 10.1046/j.1365-294X.2002.01643.x
Klintschar, M. et al. Haplotype studies support slippage as the mechanism of germline mutations in short tandem repeats. Electrophoresis 25, 3344–3348 (2004).
pubmed: 15490457
doi: 10.1002/elps.200406069
Jonika, M., Lo, J. & Blackmon, H. Mode and tempo of microsatellite evolution across 300 million years of insect evolution. Genes 11, 1–15 (2020).
doi: 10.3390/genes11080945
Shedlock, A. M. et al. Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genome. Proc. Natl. Acad. Sci. 104, 2767–2772 (2007).
pubmed: 17307883
pmcid: 1815256
doi: 10.1073/pnas.0606204104
Ferreira, G. S., Rincón, A. D., Solórzano, A. & Langer, M. C. Review of the fossil matamata turtles: Earliest well-dated record and hypotheses on the origin of their present geographical distribution. Sci. Nat. 103, 1–12 (2016).
doi: 10.1007/s00114-016-1355-2
Sumner, A. T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75, 304–306 (1972).
pubmed: 4117921
doi: 10.1016/0014-4827(72)90558-7
Gross, M. C., Schneider, C. H., Valente, G. T., Martins, C. & Feldberg, E. Variability of 18S rDNA locus among Symphysodon fishes: Chromosomal rearrangements. J. Fish Biol. 76, 1117–1127 (2010).
pubmed: 20409165
doi: 10.1111/j.1095-8649.2010.02550.x
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, 4780–4780 (1991).
pubmed: 1891373
pmcid: 328734
doi: 10.1093/nar/19.17.4780
Viana, P. F. et al. Is the karyotype of neotropical boid snakes really conserved? Cytotaxonomy, chromosomal rearrangements and karyotype organization in the Boidae family. PLoS ONE 11, 1–16 (2016).
doi: 10.1371/journal.pone.0160274
Viana, P. F., Ezaz, T., Cioffi, M. D. 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 10, 1–15 (2019).
doi: 10.3390/genes10040288
Zwick, M. S. et al. A rapid procedure for the isolation of C
pubmed: 18464813
doi: 10.1139/g97-020
Ferreira, A. M. V. et al. Cytogenetic Analysis of Panaqolus tankei Cramer & Sousa, 2016 (Siluriformes, Loricariidae), an Ornamental Fish Endemic to Xingu River, Brazil. Cytogenet. Genome Res. 161, 187–194 (2021).
pubmed: 33744896
doi: 10.1159/000514061
Levan, A., Fredga, K. & Sandberg, A. A. Nomenclature for centromeric position on chromosomes. Hereditas 52, 201–220 (1964).
doi: 10.1111/j.1601-5223.1964.tb01953.x