Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography

Molecular Phylogenetics and Evolution - Tập 148 - Trang 106823 - 2020
Mario Vargas-Ramírez1,2,3, Susana Caballero4, Mónica A. Morales-Betancourt5, Carlos A. Lasso5, Laura Amaya4, José Gregorio Martínez6,7, Maria das Neves Silva Viana7, Richard C. Vogt8, Izeni Pires Farias7, Tomas Hrbek7, Patrick D. Campbell9, Uwe Fritz3
1Estación de Biología Tropical Roberto Franco (EBTRF), Universidad Nacional de Colombia, Villavicencio, Colombia
2Biodiversidad y Conservación Genética, Instituto de Genética, Universidad Nacional de Colombia, Bogotá, Colombia
3Museum of Zoology, Senckenberg Dresden, A. B. Meyer Building, Dresden, Germany
4Laboratorio de Ecología Molecular de Vertebrados Acuáticos-LEMVA, Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
5Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Programa Ciencias de la Biodiversidad, Línea de Recursos Hidrobiológicos, Pesqueros Continentales y Fauna Silvestre, Bogotá, Colombia
6Grupo de Investigación Biociencias, Facultad de Ciencias de la Salud, Institución Universitaria Colegio Mayor de Antioquia, Medellín, Colombia
7Laboratório de Evolução e Genética Animal, Departamento de Genetica, Universidade Federal do Amazonas, Manaus, Brazil
8Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil
9Department of Life Sciences, Darwin Centre 1, Natural History Museum, London, UK

Tài liệu tham khảo

Amaya-Calderón, 2016 Bager, 2010, Estimation of core terrestrial habitats for freshwater turtles in Southern Brazil based on nesting areas, J. Herpetol., 44, 658, 10.1670/09-036.1 Barrio-Amoros, 2006, Record de taille pour une matamata (Chelus fimbriatus) au Venezuela, Manouria, 32, 23 Baur, 1890, An apparently new species of Chelys, Amer. Nat., 24, 967 Barrère, P., 1741. Essai sur l’histoire naturelle de la France équinoxiale. Piget, Paris. Bouckaert, 2019, beast 2.5: an advanced software platform for Bayesian evolutionary analysis, PLoS Comput. Biol., 15, 10.1371/journal.pcbi.1006650 Boulenger, 1889 Burger, 2010, Arsenic, cadmium, chromium, lead, mercury, and selenium levels in blood of four species of turtles from the Amazon in Brazil, J. Toxicol. Environ. Health Part A, 73, 33, 10.1080/15287390903248877 Bruguière, 1792, Description d’une nouvelle espèce de tortue de Cayenne, J. Hist. Nat. Paris, 1, 253 Bryant, 2012, Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis, Mol. Biol. Evol., 29, 1917, 10.1093/molbev/mss086 Cadena, 2015, The first fossil skull of Chelus (Pleurodira: Chelidae, matamata turtle) from the early Miocene of Colombia, Paleontol. Electron., 18.2(32A), 1 Cadena, 2008, New material of Chelus colombiana (Testudines; Pleurodira) from the lower Miocene of Colombia, J. Vert. Paleontol., 28, 1206, 10.1671/0272-4634-28.4.1206 Clement, 2000, tcs: a computer program to estimate gene genealogies, Mol. Ecol., 9, 1657, 10.1046/j.1365-294x.2000.01020.x Cooper, 1995, Basin development and tectonic history of the Llano Basin, Eastern Cordillera, and middle Magdalena Valley, Colombia, AAPG Bull., 79, 1421 Daudin, 1801 Díaz de Gamero, 1996, The changing course of the Orinoco River during the Neogene: a review, Palaeogeogr. Palaeoclimatol. Palaeoecol., 123, 385, 10.1016/0031-0182(96)00115-0 Drummond, 2007, beast: Bayesian evolutionary analysis by sampling trees, BMC Evol. Biol., 7, 214, 10.1186/1471-2148-7-214 Earl, 2012, structure harvester: a website and program for visualizing structure output and implementing the Evanno method, Conserv. Genet. Resour., 4, 359, 10.1007/s12686-011-9548-7 Ernst, 1989 Escobar, 2015, Delimiting evolutionarily significant units of the fish, Piaractus brachypomus (Characiformes: Serrasalmidae), from the Orinoco and Amazon River Basins with insight on routes of historical connectivity, J. Hered., 105, 428, 10.1093/jhered/esv047 Evanno, 2005, Detecting the number of clusters of individuals using the software structure: a simulation study, Mol. Ecol., 14, 2611, 10.1111/j.1365-294X.2005.02553.x Ferrara, 2017 Ferreira, 2016, Review of the fossil matamata turtles: earliest well-dated record and hypotheses on the origin of their present geographical distribution, Sci. Nat., 103, 28, 10.1007/s00114-016-1355-2 Foll, 2008, A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective, Genetics, 180, 977, 10.1534/genetics.108.092221 Fretey, 1977 Fritz, 2012, Northern genetic richness and southern purity, but just one species in the Chelonoidis chilensis complex, Zool. Scr., 41, 220, 10.1111/j.1463-6409.2012.00533.x Fritz, 2006, A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy, Zool. Scr., 35, 531, 10.1111/j.1463-6409.2006.00242.x Fritz, 2007, Checklist of chelonians of the world, Vertebr. Zool., 57, 149, 10.3897/vz.57.e30895 Fujita, 2004, Turtle phylogeny: insights from a novel nuclear intron, Mol. Phylogenet. Evol., 31, 1031, 10.1016/j.ympev.2003.09.016 Galvis, 2012, Biogeografía continental colombiana: un enfoque desde la hidrografía, 81 Garbin, 2015, Is the matamata only one species? Morphological variation and color polymorphism in the South American turtle Chelus fimbriatus (Schneider, 1783) (Pleurodira: Chelidae), PeerJ PrePrints, 3 García, 2016, Molecular systematics of the freshwater stingrays (Myliobatiformes: Potamotrygonidae) of the Amazon, Orinoco, Magdalena, Esequibo, Caribbean, and Maracaibo basins (Colombia – Venezuela): evidence from three mitochondrial genes, Mitochondrial DNA A, 27, 4479, 10.3109/19401736.2015.1101536 Gehara, 2014, High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog Dendropsophus minutus, PLoS ONE, 9, 10.1371/journal.pone.0103958 Georges, 2010, Diversity of Australasian freshwater turtles, with an annotated synonymy and keys to species, Zootaxa, 2496, 1, 10.11646/zootaxa.2496.1.1 Hammer, 2001, past: paleontological statistics software package for education and data analysis, Paleontol. Electron., 4, 4 Hoorn, 1995, Andean tectonics as a cause for changing drainage patterns in Miocene northern South America, Geology, 23, 237, 10.1130/0091-7613(1995)023<0237:ATAACF>2.3.CO;2 Hoorn, 2010, Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity, Science, 330, 927, 10.1126/science.1194585 Hrbek, T., Martínez, J.G., Hernández-Rangel, S.M., Bertuol, F., de Assunção, E.N., Canton, R. de C., Astolfi-Filho, S., Farias, I.P., 2020. Optimizing Next Generation Sequencing for biodiversity studies on the Ion Torrent PGM: an in silico and in vitro analysis. PeerJ (accepted). Iverson, 1992 Jombart, 2008, adegenet: a R package for the multivariate analysis of genetic markers, Bioinformatics, 24, 1403, 10.1093/bioinformatics/btn129 Joyce, 2013, A divergence dating analysis of turtles using fossil calibrations: an example of best practices, J. Paleontol., 87, 612, 10.1666/12-149 Kass, 1995, Bayes factors, J. Am. Stat. Assoc., 90, 773, 10.1080/01621459.1995.10476572 Kehlmaier, 2019, Mitogenomics of historical type specimens of Australasian turtles: clarification of taxonomic confusion and old mitochondrial introgression, Sci. Rep., 9, 5841, 10.1038/s41598-019-42310-x Kindler, 2012, Molecular phylogeny of African hinge-back tortoises (Kinixys): implications for phylogeography and taxonomy (Testudines: Testudinidae), J. Zool. Syst. Evol. Res., 50, 192, 10.1111/j.1439-0469.2012.00660.x Kindler, 2016, Comparative phylogeographies of six species of hinged terrapins (Pelusios spp.) reveal discordant patterns and unexpected differentiation in the P. castaneus/P. chapini complex and P. rhodesianus, Biol. J. Linn. Soc., 117, 305, 10.1111/bij.12647 King, 1989 Kumar, 2016, mega7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054 Lanfear, 2012, partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses, Mol. Biol. Evol., 29, 1695, 10.1093/molbev/mss020 Lasso, 2018, 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 Colomb., 19, 147, 10.21068/c2018.v19n01a10 Leaché, 2014, Species delimitation using genome-wide SNP data, Syst. Biol., 63, 534, 10.1093/sysbio/syu018 Lemell, 2010, The feeding apparatus of Chelus fimbriatus (Pleurodira; Chelidae) – adaptation perfected?, Amphibia-Reptilia, 31, 97, 10.1163/156853810790457803 Lemell, 2002, Feeding patterns of Chelus fimbriatus (Pleurodira: Chelidae), J. Exp. Biol., 205, 1495, 10.1242/jeb.205.10.1495 Lundberg, 1998, The stage for neotropical fish diversification: a history of tropical South American rivers, 13 Medem, 1960, Datos zoogeográficos y ecológicos sobre los Crocodylia y Testudinata de los Ríos Amazonas, Putumayo y Caqueta, Caldasia, 8, 341 Michels, 2018, Red-headed Amazon river turtles in Venezuela and Colombia: population separation and connection along the famous route of Alexander von Humboldt, Zoology, 130, 67, 10.1016/j.zool.2018.07.004 Ministerio de Ambiente y Desarrollo Sostenible, 2012. Estrategia nacional para la prevención y control al tráfico ilegal de especies silvestres: diagnóstico y plan de acción ajustado. Ministerio de Ambiente y Desarrollo Sostenible, Bogotá. Moritz, 1994, Application of mitochondrial DNA analysis in conservation: a critical review, Mol. Ecol., 3, 401, 10.1111/j.1365-294X.1994.tb00080.x Nylander, 2004, Bayesian phylogenetic analysis of combined data, Syst. Biol., 53, 47, 10.1080/10635150490264699 Páez, 2012 Parham, 2012, Best practices for justifying fossil calibrations, Syst. Biol., 61, 346, 10.1093/sysbio/syr107 Petzold, 2014, A revision of African helmeted terrapins (Testudines: Pelomedusidae: Pelomedusa), with descriptions of six new species, Zootaxa, 3795, 523, 10.11646/zootaxa.3795.5.2 Pinto-Sánchez, 2015, Molecular phylogenetics and biogeography of the Neotropical skink genus Mabuya Fitzinger (Squamata: Scincidae) with emphasis on Colombian populations, Mol. Phylogenet. Evol., 93, 188, 10.1016/j.ympev.2015.07.016 Praschag, 2007, Phylogeny and taxonomy of endangered South and South-east Asian freshwater turtles elucidated by mtDNA sequence variation (Testudines: Geoemydidae: Batagur, Callagur, Hardella, Kachuga, Pangshura), Zool. Scr., 36, 429, 10.1111/j.1463-6409.2007.00293.x Pritchard, 2000, Inference of population structure using multilocus genotype data, Genetics, 155, 945, 10.1093/genetics/155.2.945 Pritchard, 1984, Piscivory in turtles, and evolution of the long-necked Chelidae, 87 Pritchard, 2008, Chelus fimbriata (Schneider 1783) – Matamata turtle, 1 Pritchard, P.C.H., Trebbau, P., 1984. The Turtles of Venezuela. Society for the Study of Amphibians and Reptiles, Athens, OH. de Queiroz, 1999, The General Lineage Concept of species and the defining properties of the species category, 49 de Queiroz, 2007, Species concepts and species delimitation, Syst. Biol., 56, 879, 10.1080/10635150701701083 Rambaut, A., Drummond, A.J., 2007. tracer v1.4. Available at: http://beast.bio.ed.ac.uk/Tracer. Renza-Millán, 2019, Mitochondrial DNA diversity and population structure of the ocellate freshwater stingray Potamotrygon motoro (Müller & Henle, 1841) (Myliobatiformes: Potamotrygonidae) in the Colombian Amazon and Orinoco Basins, Mitochondrial DNA A, 30, 466, 10.1080/24701394.2018.1546300 Ronquist, 2012, mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space, Syst. Biol., 61, 539, 10.1093/sysbio/sys029 Rosenberg, 2004, distruct: a program for the graphical display of population structure, Mol. Ecol. Notes, 4, 137, 10.1046/j.1471-8286.2003.00566.x Rueda-Almonacid, 2007 Salas-Gismondi, 2015, A Miocene hyperdiverse crocodilian community reveals peculiar trophic dynamics in proto-Amazonian mega-wetlands, Proc. R. Soc. B, 282, 20142490, 10.1098/rspb.2014.2490 Sánchez-Villagra, 1995, Consideraciones sobre la sistemática de las tortugas del género Chelus (Pleurodira: Chelidae) y nuevas evidencias fósiles del Mioceno de Colombia y Venezuela, Ameghiniana, 32, 159 Sánchez-Villagra, 1995, Geographic variation in the matamata turtle, Chelus fimbriatus, with observations on its shell morphology and morphometry, Chelon. Conserv. Biol., 1, 293 Schmidt, 1966, Morphologische Unterschiede bei Chelus fimbriatus verschiedener Herkunft, Salamandra, 2, 74 Schneider, J.G., 1783. Allgemeine Naturgeschichte der Schildkröten, nebst einem systematischen Verzeichnisse der einzelnen Arten und zwey Kupfern. J.G. Müller, Leipzig. Schneider, 2010, Mercury levels in muscle of six species of turtles eaten by people along the Rio Negro of the Amazon Basin, Arch. Environ. Contam. Toxicol., 58, 444, 10.1007/s00244-009-9358-z Seddon, 1997, Phylogenetic relationships of chelid turtles (Pleurodira: Chelidae) based on mitochondrial 12S rRNA gene sequence variation, Mol. Phylogenet. Evol., 7, 55, 10.1006/mpev.1996.0372 Shaffer, 2017, 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, 10.1016/j.ympev.2017.07.006 Stamatakis, 2006, RAxML-VI-HPC: Maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics, 22, 2688, 10.1093/bioinformatics/btl446 Stamatakis, 2014, RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics, 30, 1312, 10.1093/bioinformatics/btu033 Torstrom, 2014, Shedding subspecies: the influence of genetics on reptile subspecies taxonomy, Mol. Phylogenet. Evol., 76, 134, 10.1016/j.ympev.2014.03.011 2017 Untergasser, 2012, Primer3-new capabilities and interfaces, Nucleic Acids Res., 40, 10.1093/nar/gks596 Vallinoto, 2010, Phylogeny and biogeography of the Rhinella marina species complex (Amphibia, Bufonidae) revisited: implications for Neotropical diversification hypotheses, Zool. Scr., 39, 128, 10.1111/j.1463-6409.2009.00415.x Vargas-Ramírez, 2017, Reptiles Vargas-Ramírez, 2010, Deep genealogical lineages in the widely distributed African helmeted terrapin: evidence from mitochondrial and nuclear DNA (Testudines: Pelomedusidae: Pelomedusa subrufa), Mol. Phylogenet. Evol., 56, 428, 10.1016/j.ympev.2010.03.019 Wang, 2012, The complete mitochondrial genome sequences of Chelodina rugosa and Chelus fimbriata (Pleurodira: Chelidae): implications of a common absence of initiation sites (OL) in pleurodiran turtles, Mol. Biol. Rep., 39, 2097, 10.1007/s11033-011-0957-1 Wermuth, 1961 Wermuth, 1977, Testudines, Crocodylia, Rhynchocephalia, Tierreich, 100, 1 Wesselingh, 2001, Lake Pebas: a palaeoecological reconstruction of a Miocene, long-lived lake complex in western Amazonia, Cainozoic Res., 1, 35 Wilson, 2011, Evolution and phylogenetic signal of growth trajectories: the case of chelid turtles, J. Exp. Zool. B, 316, 50, 10.1002/jez.b.21380 Winemiller, 2011, The Vaupes arch and Casiquiare canal, barriers and passages, 225 Wood, 1976, Two new species of Chelus (Testudines: Pleurodira) from the late Tertiary of northern South America, Breviora, 435, 1 Ye, 2012, Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction, BMC Bioinf., 13, 134, 10.1186/1471-2105-13-134