Abstract
Xenarthra (sloths, anteaters, and armadillos) are the quintessential South American mammals. Among the xenarthrans, sloths constitute the most diverse paleontologically with almost 100 fossil genera recorded. However, this abundant sloth fauna in the Americas became extinct around 10,000 years ago. Only six species belonging to two genera, Bradypus (four three-toed sloth species) and Choloepus (two two-toed sloth species) are alive today in Central and South America. Bradypus variegatus is the sloth species with the widest geographical distribution in the Neotropics. Some regional population genetics have been reported, especially in Brazil, but with limited sample sizes. Herein, we sequenced 77 samples of Bradypys variegatus (Panama, Colombia, Venezuela, Peru, Bolivia, and Brazil; 65 new samples and 12 from GenBank), plus one B. tridactylus, one B. pygmaeus, and five B. torquatus (one new and four from GenBank) at the mitochondrial (mt) control region. Additionally, 25 of these samples, representing the four species, were sequenced for the entire mitochondrial genome. Our results indicate that there are at least six main genetically different haplogroups of B. variegatus. They are the trans-Andean, western Amazon (with some other internal groups), Tapajos River, Tocantins River, Negro River, and the Brazilian eastern Atlantic forest (with two recognizable sub-groups in northern and southern areas) ones, with the ancestor of the trans-Andean haplogroup the first to diverge. A very strong genetic heterogeneity and a striking spatial pattern were detected among these different geographical areas, with the trans-Andean, western Amazon, and Tocantins populations showing the highest levels of genetic diversity, meanwhile the Tapajos and the Brazilian eastern populations yielding lower levels of genetic diversity. The following conclusions were as follows: 1) B. torquatus should be considered as a different genus (Scaeopus) because of its extreme genetic differences from other Bradypus taxa as was previously claimed by other authors; 2) B. pygmaeus is not a recent species adapted to Holocene island environments from the Central America B. variegatus group; and 3) if we adopt a strict version of the Phylogenetic Species Concept (PSC), the highly significant monophyletic clade of the trans-Andean B. variegatus population should be defined as a valid and differentiated species of three-toed sloth. However, we are reluctant to define this population as a new species until new data shows possible strong karyotype differences and/or pre- or post-zygote reproductive barriers (Biological Species Concept, BSC) between the trans and the cis-Andean populations of the three-toed brown-throated sloth.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723
Alston ER (1880) Biologia Centrali-Americana. Mammalia. Vol. 1. Taylor and Francis, London
Anderson RP, Handley CO (2001) A new species of three-toed sloth (Mammalia: Xenarthra) from Panama, with a review of the genus Bradypus. Proc Biol Soc Wash 114: 1–33
Anderson RP, Handley CO (2002) Dwarfism in insular sloths: biogeography, selection, and evolutionary rate. Evolution 56: 1045–1058
Arnason U, Gullberg A, Janke, A (1997) Phylogenetic analyses of mitochondrial DNA suggest a sister group relationship between Xenarthra (Edentata) and ferungulates. Mol Biol Evol 14: 762–768
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeographic: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18: 489–522
Barros MC, Sampaio I, Schneider H (2003) Phylogenetic analysis of 16S mitochondrial DNA data in sloths and anteaters. Genet Mol Biol 26: 5–12
Barros M C, Sampaio I, Schneider H (2008) Novel 12S mtDNA findings in sloths (Pilosa, Folivora) and anteaters (Pilosa, Vermilingua) suggest a true case of long branch attraction. Genet Mol Biol 31: 793–799
Bates JM, Hackett SJ, Cracraft J (1998) Area relationships in the Neotropical lowlands: an hypothesis based on raw distributions of passerine birds. J Biogeogr 25: 783–793
Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16: 314–321
Boubli JP, Rylands AB, Farias IP, Alfaro ME, Lynch-Alfaro JW (2012) Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys. Am J Primatol 74: 381–393
Britton SW, Kline RF (1939) Augmentation of activity in the sloth by adrenal extract, emotion and other conditions. Am J Physiol 127: 127–130
Brouns G, De Wulf A, Constales D (2003) Delaunay triangulation algorithms useful for multibeam echosounding. J Surv Eng 129:79–84
Cabrera A (1958) Catálogo de los mamíferos de América del Sur. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” Buenos Aires Argentina Zoologia 4: 1–308
Cartelle C (1994) Tempo passado. Mamíferos do Pleistoceno em Minas Gerais. Editora Palco, Belo Horizonte
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552
Coates AG, Obando JA (1996) The geologic evolution of the Central American isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and Environment in Tropical America. University of Chicago Press, Chicago, pp 21–56
Costa LP (2003) The historical bridge between the Amazon and the Atlantic forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30: 71–86
Couzzol MA, Clozato CL, Holanda EC, Rodrigues FHG, Nienow S, Thoisy B, Redondo RAF, Santos FR (2013) A new species of tapir from the Amazon. J Mammal 94: 1331–1345
Cracraft J (1983) Species concepts and speciation analysis. In: Johnston RJ (ed) Current Ornithology. Vol I. Plenum Press, New York, pp 159–187
Da Silva JMC, Rylands AB, Fonseca GAB (2005) The fate of the Amazonian areas of endemism. Conserv Biol 19: 689–694
Delsuc F, Vizcaíno SF, Douzery EJP (2004) Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evol Biol 4: 11
De Vivo M, Carmignotto AP (2004) Holocene vegetation change and the mammal faunas of South America and Africa. J Biogeogr 31: 943–957
Ditchfield AD (2000) The comparative phylogeography of Neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals. Mol Ecol 9: 1307–1318
Dobigny G, Yang F, O’Brien P, Volobouev V, Kovacs A, Pieczarka J, Ferguson-Smith M, Robinson T (2005) Low rate of genomic repatterning in Xenarthra inferred from chromosome painting data. Chromosome Res 13: 651–663
Douzery E, Randi E (1997) The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol Biol Evol 14: 1154–1166
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969–1973
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571–2581
Engelmann GF (1985) The phylogeny of the Xenarthra. In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths and Vermilinguas. Smithsonian Institution Press, Washington and London, pp 51–64
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10: 564–567
Farris DW, Jaramillo C, Bayona G, Restrepo-Moreno SA, Montes C, Cardona A, Mora A, Speakman RJ, Glascock MD, Valencia V (2011) Fracturing of the Panamanian isthmus during initial collision with South America. Geology 39: 1007–1010
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133: 693–709
Galtier N, Enard D, Radondy Y, Bazin E, Belkhir K (2006) Mutation hotspots in mammalian mitochondrial DNA. Genome Res 16: 215–222
Gardner AL (2005) Order Pilosa. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd ed. Johns Hopkins University Press, Baltimore, 100–103
Gardner AL (2008) Magnorder Xenarthra. In: Gardner AL (ed) Mammals of South America: Volume 1 Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, pp 127–128
Gibb GC, Condamine FL, Kuch M, Enk J, Moraes-Barros N, Superina M, Poinar H N, Delsuc F (2016) Shotgun mitogenomics provides a reference phylogenetic framework and timescale for living xenarthrans. Mol Biol Evol 33: 621–642
Goldman EA (1913) Descriptions of new mammals from Panama and Mexico. Smithsonian Misc Coll 60: 1–20
Gray JE (1871) On a new species of three-toed sloth from Costa Rica. Ann Mag Nat Hist Series 4 7: 302
Gregory-Wodzicki KM (2000) Uplift history of the central and northern Andes: a review. Geol Soc Am Bull 112: 1091–1105
Guschanski K, Krause J, Sawyer S, Valente LM, Bailey S, Finstermeier K, Sabin R, Gilissen E, Sonet G, Nagy ZT, Lenglet G, Mayer F, Savolainen V (2013) Next-generation museomics disentangles one of the largest primate radiations. Syst Biol 62: 539–554
Haffer J (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodiversity and Evolution 6: 451–476
Haffer J (2008) Hypotheses to explain the origin of species in Amazonia. Braz J Biol 68: 917–947
Harpending HC (1994) Signature and ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biol 66: 591–600
Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) Genetic structure of ancient human populations. Current Anthropol 34: 483–496
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160–174
Hautier LG, Eastwood BB, Lane J (2014) Patterns of morphological variation of extant sloth skulls and their implication for future conservation efforts. Anatomical Record 297: 979–1008
Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927–931
Hrbek T, da Silva VMF, Dutra N, Gravena W, Martin AR, Farias IP (2014) A new species of river dolphin from Brazil or: how little do we know our biodiversity. PLoS One 9: 1–12
Hudson R, Boos D, Kaplan N (1992) A statistical test for detecting population subdivision. Mol Biol Evol 9 : 138–151
Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53: 904–913
International Commission on Stratigraphy (2007) International Stratigraphic Chart. http://www.sratigraphy.org/chus.pdf
Jorge W, Orsi-Souza A, Best R (1985) The somatic chromosomes of Xenarthra. In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths and Vermilinguas. Smithsonian Institution Press, Washington and London, pp 121–129
Jorge W, Pereira HRJ (2008) Chromosomal studies in the Xenarthra. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 196–204
Jorge W, Pinder L (1990) Chromosome study on the maned sloth Bradypus torquatus (Bradypodidae, Xenarthra). Cytobios 62: 21–25
Kaviar S, Shockey J, Sundberg P (2012) Observations on the endemic pygmy three-toed sloth, Bradypus pygmaeus of Isla Escudo de Veraguas, Panama. PLoS One 7: e49854. doi:https://doi.org/10.1371/journal.pone.0049854
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120
Lara-Ruiz P, Chiarello A, Santos F (2008) Extreme population divergence and conservation implications for the rare endangered Atlantic Forest sloth, Bradypus torquatus (Pilosa: Bradypodidae). Biol Conserv 141: 1332–1342
Lessa EP, Van Valkenburgh B, Fariña RA (1997) Testing hypotheses of differential mammalian extinctions subsequent to the great American biotic interchange. Palaeogeogr Palaeoclimatol Palaeoecol 135: 157–162
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. doi: https://doi.org/10.1093/bioinformatics/btp187
Long A, Martin PS (1974) Death of North American ground sloths. Science 186: 638–640
Lönnberg E (1942) Notes on Xenarthra from Brazil and Bolivia. Arkiv Zool 34A(9): 1–58
Lyons SK, Smith FA, Brown JH (2004) Of mice, mastodons and men: human mediated extinctions on four continents. Evol Ecol Res 6: 339–358
Manel S, Schwartz ML, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76: 173–190
Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220
Marshall LG, Webb SD, Sepkoski JJ, Raup DM (1982) Mammalian evolution and the great American interchange. Science 215: 1351–1357
Mason VC, Li G, Helgen KM, Murphy WJ (2011) Efficient cross-species capture hybridization and next-generation sequencing of mitochondrial genomes from noninvasively sampled museum specimens. Genome Res 21: 1695–1704
McKenna MC, Bell SK (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York
Miller MP (2005) Alleles in space: computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96: 722–724
Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5: 245–261
Montes C, Bayona G, Cardona A, Buchs DM, Silva CA, Morón S, Hoyos N, Ramírez DA, Jaramillo CA, Valencia V (2012) Arc-continent collision and orocline formation: closing of the Central American seaway. J Geophys Res 117: B04105. doi:https://doi.org/10.1029/2011JB008959
Montes C, Cardona A, Jaramillo C, Pardo A, Silva JC, Valencia V, Ayala VC, Pérez-Angel LC, Rodriguez-Parra LA, Ramirez V, Niño H (2015) Middle Miocene closure of the Central American sea way. Science 348: 226–229
Moore W (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49: 718–726
Moraes N, Morgante J, Miyaki C (2002) Genetic diversity in different populations of sloths assessed by DNA fingerprinting. Braz J Biol 62: 503–508
Moraes-Barros N, Arteaga MC (2015) Genetic diversity in Xenarthra and its relevance to patterns of Neotropical biodiversity. J Mammal 96: 690–702
Moraes-Barros N, Miyaki CY, Morgante JS (2007) Identifying management units in non-endangered species: the example of the sloth Bradypus variegatus Schinz, 1825. Braz J Biol 6: 829–837
Moraes-Barros N, Silva JAB, Miyaki CY, Morgante JS (2006) Comparative phylogeography of the Atlantic forest endemic sloth (Bradypus torquatus) and the widespread three-toed sloth (Bradypus variegatus) (Bradypodidae, Xenarthra). Genetica 126: 189–198
Moraes-Barros N, Silva JA, Morgante JS (2011) Morphology, molecular phylogeny, and taxonomic inconsistencies in the study of Bradypus sloths (Pilosa: Bradypodidae). J Mammal 92: 86–100
Morgan C, Foster PG, Webb A, Pisani D, McInerney JO, O’Connell M (2013) Heterogeneous models place the root of the placental mammal phylogeny. Mol Biol Evol 30: 2145–2156
Moss WE, Peery MZ, Gutiérrez-Espeleta GA, Vaughan C, Herrera G, Pauli JN (2012) Isolation and characterization of 18 microsatellite markers for the brown-throated three-toed sloth, Bradypus variegatus. Conserv Genet Resourc 4: 1037–1039
Murphy WJ, Eizirik E, Johnson WJ, Zhang YP, Ryder OA, O’Brien SJ (2001a) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614–618
Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001b) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348–2351
Nabholz B, Ellegren H, Wolf JB (2012) High levels of gene expression explain the strong evolutionary constraint of mitochondrial protein-coding genes. Mol Biol Evol 30: 272–284
Nores M (1999) An alternative hypothesis for the origin of Amazonian bird diversity. J Biogeogr 26: 475–485
Nores M (2004) The implications of Tertiary and Quaternary Sea level rise events for avian distribution patterns in the lowlands of northern South America. Global Ecol Biogeogr 13: 149–162
Nylander JA (2004) MrModeltest v2. Evolutionary Biology Center, Uppsala University
Oliveira E, Bergqvist L (1998) A new Paleocene armadillo (Mammalia, Dasypodoidea) from the Itaboraí Basin, Brazil. Paleógeno de América del Sur y de la Península Antártica, Asociación Paleontológica Argentina, Publicación especial 5 30: 35-40
Patterson B, Pascual R (1972) The fossil mammal fauna of South America. In: Keast A, Erk FC, Glass B (Eds) Evolution, Mammals and Southern Continents. State University of New York Press, Albany, pp 247–309
Paula-Couto C (1979) Tratado de paleomastozoologia. Academia Brasileira de Ciencias, Rio de Janeiro
Pellegrino KCM, Rodrigues MT, Waite AN, Morando M, Yassuda YY, Sites JW (2005) Phylogeography and species limits in the Gymnodactylus darwinii complex (Gekkonidae, Squamata): genetic structure coincides with river systems in the Brazilian Atlantic forest. Biol J Linn Soc 85: 13–26
Philippi RA (1870) Ueber ein neues Faulteir. Archiv für Naturgeschichte 1870: 263–267
Pinder L (1993) Body measurements, karyotype, and birth frequencies of maned sloth (Bradypus torquatus). Mammalia 57: 43–48
Pinto-da-Rocha R, Da Silva MB (2005) Faunistic similarity and historic biogeography of the harvestmen of southern and southeastern Atlantic rainforest of Brazil. J Arach 33: 290–299
Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53: 793–808
Raaum RL, Sterner KN, Noviello CM, Stewart C-B, Disotell TR (2005) Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J Hum Evol 48: 237–257
Rambaut A (2012) FigTree v1.4. http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Drummond AJ (2013a) LogCombiner v1.8.0. http://beast.bio.ed.ac.uk/
Rambaut A, Drummond AJ (2013b) TreeAnnotator v1.8.0. http://beast.bio.ed.ac.uk/
Rambaut A, Suchard MA, Xie W, Drummond AJ (2013) Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092–2100
Reyes A, Gissi C, Pesole G, Saccone C (1998) Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol Biol Evol 15: 957–966
Rogers AR, Fraley AE, Bamshad MJ, Watkins WS, Jorde LB (1996) Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol 13: 895–902
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9: 552–569
Romiguier J, Ranwez V, Delsuc F, Galtier N, Douzery EJP (2013) Less is more in mammalian phylogenomics: AT-rich genes minimize tree conflicts and unravel the root of placental mammals. Mol Biol Evol 30: 2134–2144
Ruiz-García M (1993) Analysis of the evolution and genetic diversity within and between Balearic and Iberian cat populations. J Hered 84: 173–180
Ruiz-García M (1994) Genetic profiles from coat genes of natural Balearic cat populations: an eastern Mediterranean and North-African origin. Genet Sel Evol 26: 39–64
Ruiz-García M (1997) Genetic relationships among some new cat populations sampled in Europe: a spatial autocorrelation analysis. J Genet 76: 1–24
Ruiz-García M (1999) Genetic structure of different cat populations in Europe and South America at a microgeographic level: importance of the choice of an adequate sampling level in the accuracy of population genetics interpretations. Genet Mol Biol 22: 493–505
Ruiz-García M (2005) The use of several microsatellite loci applied to 13 Neotropical primates revealed a strong recent bottleneck event in the woolly monkey (Lagothrix lagotricha) in Colombia. Primate Report 71: 27–55
Ruiz-García M, Alvarez D (2000) Genetic microstructure in two Spanish cat populations I: genic diversity, gene flow and selection. Genes Genet Syst 75: 269–280
Ruiz-García M, Chacón D, Plese T, Schuler I, Shostell JM (2018) Mitogenomics phylogenetic relationships of the current sloth’s genera and species (Bradypodidae and Megalonychidae). Mitochondrial DNA Part A 29: 281–299
Ruiz-García M, Klein KK (1997) Genetic structure of domestic cat populations (Felis catus) at micro and macrogeographical levels: two examples (Catalonia, Spain, and mid-western USA). J Genet 76: 99–114
Santos TMS (1977) Osteologia craniana de Bradypus Linnaeus, 1758 e reavaliacao do genero Scaeopus Peters, 1865. Master Thesis. Universidade Federal do Rio Grande do Sul, 178 pp
Sambrock J, Fritsch E, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edition. V1. Cold Spring Harbor laboratory Press, New York
Schwarz GE (1978) Estimating the dimension of a model. Ann Statistics 6: 461–464
Silva SM (2013) Contribuições para a conservação de Bradypus variegatus (preguiça comum): processos históricos e demográficos moldando a diversidade nuclear. Ph.D. dissertation, Universidade de São Paulo, São Paulo
Simonsen K, Churchill G, Aquadro C (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413–429
Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extension of the Mantel test of matrix corresponde. Syst Zool 35: 627–632
Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–1243
Steiner CC, Houck ML, Ryder OA (2011) Species identification and chromosome variation of captive two-toed sloths. Zoo Biol 29: 1–13
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564–577
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis, version 6.0. Mol Biol Evol 30: 2725–2729
Thalmann O, Hebler J, Poinar HN, Paabo S, Vigilant L (2004) Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other apes. Mol Ecol 13: 321–335
Thomas O (1917) Some notes on three-toed sloths. Ann Mag Nat Hist Series 8 19: 352–357
Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27: 171–180
Vanzolini PE (1988) Distributional patterns of South American lizards. In: Vanzolini PE, Hayer WR (eds) Proceedings of a Workshop on Neotropical Distribution Patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp 317–343
Van Roosmalen MGM, Frenz L, Van Hooft P, De Iongh HH (2007) A new species of living peccary (Mammalia: Tayassuidae) from the Brazilian Amazon. Bonn zool Beitr 55: 105–112
Vizcaíno SF (1994) Sistemática y Anatomía de los Astegotheriini Ameghino, 1906 (nuevo rango) (Dasypodidae, Dasypodinae). Ameghiniana 31: 3–13
Vizcaíno SF, Reguero MA, Goin FJ, Pascual R (1998) Antarctica as background for mammalian evolution. Paleógeno de América del Sur y de la Península Antártica, Asociación Paleontológica Argentina, Publicación especial 30: 201–211
Waddell PJ, Okada N, Hasegawa M (1999) Towards resolving the interordinal relationships of placental mammals. Syst Biol 48: 1–5
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10: 506–513
Watson DF (1992) Contouring: A Guide to the Analysis and Display of Spatial Data. Pergamon Press, New York
Wetzel RM (1982) Systematics, distribution, ecology, and conservation of south American edentates. In: Mares MA, Genoways HH (eds) Mammalian Biology in South America. Pymantuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh, pp 345–375
Wetzel RM (1985) The identification and distribution of recent Xenarthra (=Edentata). In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington and London, pp 5–21
Wetzel RM, Avila-Pires FD (1980) Identification and distribution of the recent sloths of Brazil (Edentata). Brazil J Biol 40: 831–836
Zachos FE (2016) Tree thinking and species delimitation: guidelines for taxonomy and phylogenetic terminology. Mammal Biol 81: 185–188
Acknowledgments
Thanks to Dr. Diana Alvarez, Pablo Escobar-Armel, Nicolás Lichilín, Luisa Castellanos-Mora, Kelly Luengas, and Alan Velarde for their respective help in obtaining sloth samples over the last 20 years. Thanks to Instituto von Humboldt (Villa de Leyva in Colombia; Janeth Muñoz and Andrés Cuervo), to the Peruvian Ministry of Environment, PRODUCE (Dirección Nacional de Extracción y Procesamiento Pesquero), Consejo Nacional del Ambiente and the Instituto Nacional de Recursos Naturales from Peru, to the Colección Boliviana de Fauna (Dr. Julieta Vargas) and to CITES Bolivia, to the National Environmental authority from Panama, and the Brazilian IBAMA for their role in facilitating the obtainment of collection permits in Colombia, Peru, Bolivia, Panama and Brazil. We also thank the many people of diverse Indian tribes in Peru (Bora, Shipigo-Comibo, Kishuarana and Alamas), Bolivia (Sirionó, Canichana and Chacobo), and Colombia (Tucano, Nonuya, Yuri and Yucuna), and many people in Panama and Brazil for their support in obtaining samples of Bradypus.
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Ruiz-García, M., Chacón, D., Plese, T. et al. Molecular Phylogenetics of Bradypus (Three-Toed Sloth, Pilosa: Bradypodidae, Mammalia) and Phylogeography of Bradypus variegatus (Brown-Throated Three-Toed Sloth) with Mitochondrial Gene Sequences. J Mammal Evol 27, 461–482 (2020). https://doi.org/10.1007/s10914-019-09465-w
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DOI: https://doi.org/10.1007/s10914-019-09465-w