Skip to main content
SpringerLink
Log in

Molecular Evolution (Mitochondrial and Nuclear Microsatellites Markers) in the Andean Bear (Tremarctos ornatus; Ursidae, Carnivora): How Many ESUs Are There?

  • Chapter
  • First Online:
Conservation Genetics in Mammals

Abstract

We sequenced mitochondrial genes ND5, 12s rRNA, and COI in 302 Andean or spectacled bears (Ursidae) from Venezuela, Colombia, Ecuador, Peru, and Bolivia. Of this total, 294 of the bears were from the wild whereas the remaining eight were from zoos in Mexico, Argentina, France, and Switzerland. A subset of 127 individuals, representing the above five South American countries, was genotyped at seven nuclear microsatellites (GID, G10B, G10C, G10L, G10M, G10P, and G10X). Our results support the following: (1) There are two evolutionary significant units (ESUs), following the definition of Moritz (1994). The first (Northern Andean Clade, NAC) comprises all the bears from Venezuela, Colombia, Ecuador, and northcentral Peru, whereas the second (Southern Andean Clade, SAC) comprises the bears from southern Peru and the northern and central Bolivian Andes. The temporal split between the ESUs was estimated to have occurred around 500,000 years ago (YA). Additionally, in Bolivia, a few of the sampled Andean bears in the Santa Cruz Department were more related to NAC than to SAC; (2) The eight captive bears belonged to the NAC, and thus, individuals from the SAC could be underrepresented in international zoos; 3) Different historical demographic analyses showed signatures of significant population expansions for the species as a whole and in each one of the ESUs found. These population expansions began between 690,000 and 450,000 YA. Nevertheless, one procedure detected a population decrease in the last few hundred to few thousand years for the species as a whole and in each one of the ESUs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control AC 19:716–723

    Article  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden, Massachusetts, USA

    Google Scholar 

  • Amos W, Rubinsztein DC (1996) Microsatellite are subject to directional evolution. Nat Genet 13:390–391

    Article  CAS  PubMed  Google Scholar 

  • 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. Ann Rev Ecol Evol Syst 18:489–522

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–416

    Article  PubMed  Google Scholar 

  • Bebbington A, Humphreys D, Bury J, Lingan J, Muñoz JP, Scurrah M (2008) Mining and social movements: struggles over livelihood and rural territorial development in the Andes. World Dev 36:2888–2905

    Article  Google Scholar 

  • Clapperton C (1993) Quaternary geology and geomorphology of South America. (ed) Elsevier, Amsterdam, The Netherlands

    Google Scholar 

  • Correal G (1990) Aguazuque, Evidencias de Cazadores, Recolectores y Plantadores en la Altiplanicie de la Cordillera Oriental. (Aguazuque, Evidence of hunters, collectors and planters in the Highland of the Eastern Cordillera). Fundación de Investigaciones Arqueológicas Nacionales del Banco de la República, Bogotá, Colombia

    Google Scholar 

  • Cossíos ED, Lucherini M, Ruiz-García M, Angers B (2009) Influence of ancient glacial periods on the Andean fauna: the case of the Pampas cat (Leopardus colocolo). BMC Evol Biol 9:68–79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Crandall KA, Binindaemonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  CAS  PubMed  Google Scholar 

  • Culver M, Johnson WE, Pecon-Slattery J, O’Brien SJ (2000) Genomic ancestry of the American puma (Puma concolor). J Hered 91:186–197

    Article  CAS  PubMed  Google Scholar 

  • Dizon AE, Lockyer C, Perrin WF, Demaster DP, Sisson J (1992) Rethinking the stock concept—a phylogeographic approach. Conserv Biol 6:24–36

    Article  Google Scholar 

  • Dobzhansky T (1971) Evolutionary oscillations in Drosophila pseudoobscura. In: Ford EB (ed) Ecological genetics and evolution. Blackwell Scientific, Oxford, pp 109–133

    Chapter  Google Scholar 

  • Dollfus O (1964) Cambios climáticos cuaternarios en los Andes peruanos (Primera parte). Boletín de la Sociedad Geográfica de Lima T. LXXXIII: 65–74

    Google Scholar 

  • Duellman W (1977) Origin, evolution and dispersal of the Andean herpetofauna. Ann Meet Herepetol League (Lawrence, Kansas), pp 1–7

    Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species geographic ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Eizirik E, Bonatto SL, Johnson WE, Crawshaw PG Jr, Vié JC, Brousset DM, O’Brien SJ, Salzano FM (1998) Phylogeographic patterns and evolution of the mitochondrial DNA control region in two Neotropical cats (Mammalia, Felidae). J Mol Evol 47:613–624

    Article  CAS  PubMed  Google Scholar 

  • Eizirik E, Kim J, Menotti-Raymond M, Crawshaw PG Jr, O’Brien SJ, Johnson WE (2001) Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol Ecol 10:65–79

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H, Primmer CR, Sheldon BC (1995) Microsatellite evolution: directionality or bias? Nat Genet 11:360–362

    Article  CAS  PubMed  Google Scholar 

  • Ellengren H, Moore S, Robinson N, Byrne K, Ward W, Sheldon B (1997) Microsatellite evolution-a reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14:854–860

    Article  Google Scholar 

  • Excoffier L, Lischer HE (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

    Article  PubMed  Google Scholar 

  • Figueroa J, Stucchi M (2009) El Oso andino: Alcances sobre su historia natural. Asociación para la Investigación y la Conservación de la Biodiversidad-AICB, Lima, Perú

    Google Scholar 

  • Flores Y (1975) Excavaciones en el Mirador, Pacopampa. (Excavations in El Mirador, Pacopampa.). Seminario de Historia Rural Andina, Lima, Perú

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Article  CAS  PubMed  Google Scholar 

  • Galtier N, Enard D, Radondy Y, Bazin E, Belkhir K (2006) Mutation hotspots in mammalian mitochondrial DNA. Genome Res 16:215–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Rangel S (2012) On Andean bear (Tremarctos ornatus) natural history and conservation. Mammal Rev 42:85–119

    Article  Google Scholar 

  • Goldman D, Giri PR, O’Brien SJ (1989) Molecular genetic distance estimates among the Ursidae as indicated by one- and two-dimensional protein electrophoresis. Evolution 43:282–295

    Article  PubMed  Google Scholar 

  • Goldstein DB, Ruiz-Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harpending H (1994) Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) Genetic structure of ancient human populations. Curr Antrophol 34:483–496

    Article  Google Scholar 

  • Hudson RR, Boss DD, Kaplan NL (1992) A statistical test for detecting population subdivision. Mol Biol Evol 9:138–151

    CAS  PubMed  Google Scholar 

  • Kurtén B (1967) Pleistocene bears of North America, II: genus Arctodus, short-faced bears. Acta Zool Fenn 117:1–160

    Google Scholar 

  • Lanave CG, Preparata C, Saccone (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Mannise N, Cosse M, González S, Emmons LH, Barbanti-Duarte JM, Beccaceci MD, Maldonado JE (2018) Maned wolves retain moderate levels of genetic diversity and gene flow despite drastic habitat fragmentation. Endang Spec. Res 34:449–462

    Article  Google Scholar 

  • Marin JC, Casey CS, Kadwell M, Yaya K, Hoces D, Olazabal J, Rosadio R, Rodríguez J, Spotorno A, Bruford MW (2007) Mitochondrial phylogeography and demographic history of the Vicuna: implications for conservation. Heredity 99:70–80

    Article  CAS  PubMed  Google Scholar 

  • Menéndez-Fernández M (2013) Prehistoria reciente de la penísnsula Ibérica. Universidad Nacional de Educación a Distancia, Madrid

    Google Scholar 

  • Mitchell KJ, Bray SC, Bover P, Soibelzon L, Schubert BW, Prevosti F, Prieto A, Martin F, Austin JJ, Cooper A (2016) Ancient mitochondrial DNA reveals convergent evolution of giant short- faced bears (Tremarctinae) in North and South America. Biol Let 12:1–4. https://doi.org/10.1098/rsbl.2016.0062

    Article  CAS  Google Scholar 

  • Moore W (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726

    PubMed  Google Scholar 

  • Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Morral N, Bertrantpetit J, Estivill X (1994) The origin of the major cystic fibrosis mutation (delta F508) in European populations. Nat Genet 7:169–175

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nash WG, O’Brien SJ (1987) A comparative chromosome banding analysis of the Ursidae and their relationship to other Carnivores. Cytogenet Cell Genet 45:206–212

    Article  CAS  PubMed  Google Scholar 

  • Nylander JA (2004) MrModeltest v2. Evolutionary Biology Center, Uppsala University

    Google Scholar 

  • Orejuela J, Jorgenson J (1999) Status and management of the Spectacled bear in Colombia. In: Servheen C, Herrero S, Peyton B (eds) Bears. Status survey and conservation action plan, pp 168–179. IUCN/SSC Bear and Polar Bear Specialist Groups, Gland Switzerland and Cambridge, UK

    Google Scholar 

  • O’Ryan CE, Harley H, Bruford MW, Beaumont M, Wayne RK, Cherry MI (1998) Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Anim Conserv 1:85–94

    Article  Google Scholar 

  • Pennington RT, Dick CW (2010) Diversification of the Amazonian flora and its relation to key geological and environmental events: a molecular perspective. In: Hoorn C, Wesselingh F (eds) Amazonia, landscape and species evolution: a look into the past. Wiley-Blackwell, Oxford, pp 373–385

    Google Scholar 

  • Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489–495

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Calvert W, Stirling S, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  PubMed  Google Scholar 

  • Peña GA, Pinto M (1996) Mamíferos más comunes de sitios Precerámicos de la sabana de Bogotá. Academia Nacional de Ciencias Exactas, Físicas y Naturales, vol 6. Colección Julio Carrizosa Valenzuela, Bogotá, Colombia

    Google Scholar 

  • Peyton B (1980) Ecology, distribution, and food habits of spectacled bears, Tremarctos ornatus, in Peru. J Mammal 61:639–652

    Article  Google Scholar 

  • Peyton B (1999) Spectacled bear conservation action plan. In: Servheen C, Herrero S, Peyton B (eds) Bears. Status survey and conservation action plan, pp 157–164. IUCN/SSC Bear and Polar Bear Specialist Groups, Gland, Switzerland and Cambridge, UK

    Google Scholar 

  • Peyton B, Yerena E, Rúmiz DI et al (1998) Status of wild Andean bears and policies for their management. Ursus 10:87–100

    Google Scholar 

  • Portillo-Quintero C, Larreal J, Gonzalez I, Sanchez A, Valbuena C (2012) Forest Cover and deforestation patterns in the northern Andes (Lake Maracaibo Basin): a synoptic assessment using MODIS and Landsat imagery. Appl Geogr 35:152–163

    Article  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  PubMed  Google Scholar 

  • Rodriguez ED, Poveda FE, Rivera D et al (1986) Distribución preliminar del oso andino (Tremarctos ornatus) en Colombia. MANABA 2:1–16

    Google Scholar 

  • Rodríguez ED, Cuesta F, Goldstein I, Bracho AE, Naranjo LG, Hernandez OL (2003) Ecoregional strategy for the conservation of the spectacled bear (Tremarctos ornatus) in the northern Andes. WWF Colombia, Fundación Wii, EcoCiencia, Wildlife Conservation Society, and Red Tremarctos

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rothlisberger F (1987) 10,000 jahre gletschergeschichte der erde. Verlag Sauerlander, Aarau, Switzerland

    Google Scholar 

  • Ruiz-García M (2003) Molecular population genetic analysis of the spectacled bear (Tremarctos ornatus) in the Northern Andean Area. Hereditas 138:81–93

    Article  PubMed  Google Scholar 

  • Ruiz-García M (2006) El oso andino, evolución y conservación: una sorprendente historia contenida en sus genes. In: Avances del Programa Nacional para la conservación en Colombia del oso andino (Tremarctos ornatus). Plan de acción 2002–2016. Dirección General de Ecosistemas. Ministerio de Ambiente, Vivienda y desarrollo territorial, pp 19–27. Bogotá, Colombia

    Google Scholar 

  • Ruiz-García M (2007) Genética de Poblaciones: Teoría y aplicación a la conservación de mamíferos neotropicales (Oso andino y delfín rosado). Bol Real Soc Esp Hist Nat 102(1–4):99–126

    Google Scholar 

  • Ruiz-García M (2013) The genetic demography history and phylogeography of the Andean bear (Tremarctos ornatus) by means of microsatellites and mtDNA markers. In: Ruiz-García M, Shostell JM (eds) Molecular population genetics, evolutionary biology and conservation of Neotropical carnivores. Nova Science Publishers, New York, pp 129–158

    Google Scholar 

  • Ruiz-García M, Orozco-terWengel P, Payán E, Castellanos A (2003) Genética de Poblaciones molecular aplicada al estudio de dos grandes carnívoros (Tremarctos ornatus—Oso andino, Panthera onca- jaguar): lecciones de conservación. Bol Real Soc Esp Hist Nat 98(1–4): 135–158

    Google Scholar 

  • Ruiz-García M, Orozco-terWengel P, Castellanos A, Arias L (2005) Microsatellite analysis of the spectacled bear (Tremarctos ornatus) across its range distribution. Genes Genet Syst 80:57–69

    Article  PubMed  Google Scholar 

  • Ruiz-García M, Cossíos D, Lucherini M, Yáñez J, Pinedo M, Angers B (2013a) Population genetics and spatial structure in two Andean cats (the Pampas cat, Leopardus pajeros and the Andean mountain cat, L. jacobita) by means of nuclear and mitochondrial markers and some notes on skull biometrics. In: Ruiz-García M, Shostell JM (eds) Molecular population genetics, phylogenetics, evolutionary biology and conservation of the neotropical carnivores, pp. 187–244. Nova Science Publishers, New York

    Google Scholar 

  • Ruiz-García M, Vásquez C, Murillo M, Pinedo M, Álvarez D (2013b) Population genetics and phylogeography of the largest wild cat in the Americas: An analysis of the jaguar by means of microsatellites and mitochondrial gene sequences. In: Ruiz-García M, Shostell JM (eds) Molecular population genetics, phylogenetics, evolutionary biology and conservation of the neotropical carnivores. Nova Science Publishers, New York, pp 413–464

    Google Scholar 

  • Ruiz-García M, Castellanos A, Bernal LA, Pinedo-Castro M, Kaston F, Shostell JM (2016) Mitogenomics of the mountain tapir (Tapirus pinchaque, Tapiridae, Perissodactyla, Mammalia) in Colombia and Ecuador: phylogeography and insights into the origin and systematics of the South American tapirs. Mammal Biol 81:163–175

    Article  Google Scholar 

  • Ruiz-García M, Lichilín-Ortíz N, Mejia Y, Ortega JM, Shostell JM (2017a) Mitochondrial population genetics inferences about the phylogeography and systematics of the tayra (Eira barbara, Mustelidae, Carnivora). Adv Genet Res 17:63–106

    Google Scholar 

  • Ruiz-García M, Escobar-Armel P, Thoisy B, Martínez-Agüero M, Pinedo-Castro M, Shostell JM (2018) Biodiversity in the Amazon: origin hypotheses, intrinsic capacity of species co- lonization, and comparative phylogeography of river otters (Lontra longicaudis and Pteronura brasiliensis, Mustelidae, Carnivora) and pink river dolphin (Inia sp, Iniidae, Cetacea). J Mammal Evol 25:213–240

    Article  Google Scholar 

  • Ruiz-García M, Jaramillo MF, Shostell JM (2019) Mitochondrial phylogeny of kinkajous (Procyonidae, Carnivora): maybe not a single ESU. J Mammal 100:1631–1652

    Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Saillard J, Forster P, Lynnerup N, Bandelt H-J, Norby S (2000) mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am J Hum Genet 67:718–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrock J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. V1. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sánchez-Mercado A (2008) Efecto de la estructura espacial en la persistencia de poblaciones fragmentadas: El oso andino (Tremarctos ornatus) en Venezuela como caso de estudio. Centro de Estudios Avanzados, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela

    Google Scholar 

  • Servant M, Fontes TC, Rieu M, Saliege JF (1981) Phases climatiques arides holocenes dans le Sud- Ouest de l’ Amazonie (Bolivie). CR Acad Sci Ser 2 Paris 292: 1295–1297

    Google Scholar 

  • Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65

    Article  PubMed  Google Scholar 

  • Soibelzon L (2002) Los Ursidae (Carnivora, Fissipedia) fósiles de la República Argentina. Aspectos Sistemáticos y Paleoecológicos. (The fossil Ursidae (Carnivora, Fissipedia) from Argentina). Ph.D. Dissertation, Universidad Nacional de La Plata, La Plata, Argentina

    Google Scholar 

  • Soibelzon LH (2004) Revisión sistemática de los Tremarctinae (Carnivora, Ursidae) fósiles de América del Sur. Rev Mus Argent Cienc Nat 6:107–133

    Google Scholar 

  • Soibelzon LH, Prevosti F (2007) Los Carnívoros (Carnivora, Mammalia) terrestres del Cuaternario de América del Sur. In: Pons GX, Vicens D (eds) Geomorfología litoral i Quaternari. Homenatge a D. Joan Cuerda Barceló. Mon Societat d’Historia Natural de les Balears 12: 5–12

    Google Scholar 

  • Soibelzon LH, Prevosti F (2013) Fossils of South American land carnivores (Carnivora, Mammalia). In: Ruiz-García M, Shostell JM (eds) Molecular population genetics, evolutionary biology and biological conservation of Neotropical carnivores. Nova Science Publisher, New York, NY, pp 509–530

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:1243–2688

    Article  CAS  Google Scholar 

  • Stucchi M, Salas-Gismondi R, Baby P, Guyot J-L, Shockey BJ (2009) A 6,000+ year old specimen of a spectacled bear from an Andean cave in Perú. Ursus 20:63–68

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tchaicka L, Eizirik E, De Oliveira T, Cándido JF, Freitas T (2006) Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Mol Ecol 16:819–838

    Article  CAS  Google Scholar 

  • Thompson LG, Mosley E, Davies ME, Lin PN, Henderson KA, Coledal J, Bolzan JF, Liu KB (1995) Huascarán, Perú. Science 269:46–50

    Article  CAS  PubMed  Google Scholar 

  • Trinca CS, DeThoisy B, Rosas FCW, Walderman HF, Koepfli KP, Vianna JA, Eizirik E (2012) Phylogeography and demographic history of the Neotropical otter (Lontra longicau-dis). J Hered 103:479–492

    Article  PubMed  Google Scholar 

  • Van der Hammen T (2001) Paleoecology of Amazonia. In: Guimaraes-Vieira IC, Silva JMC, Oren DC, D’Incao MA (eds) Diversidade biológica e cultural da Amazonia. Museum Paraense Emilio Goeldi, Belem, Brazil, pp 19–44

    Google Scholar 

  • Van der Hammen T, Cleff AM (1992) Holocene changes of rainfall and river discharge in northern South America and the El Niño phenomenon. Erdkunde 46:252–256

    Google Scholar 

  • Viteri MP, Waits LP (2009) Identifying polymorphic microsatellite loci for Andean bear research. Ursus 20: 102–108

    Article  Google Scholar 

  • Waits LP, Sullivan J, O’Brien S, Ward RH (1999) Rapid radiation events in the family Ursidae indicated by likelihood phylogenetic estimation from multiple fragments of mtDNA. Mol Phylogenet Evol 13:82–92

    Article  CAS  PubMed  Google Scholar 

  • Waits LP, Taberlet P, Swenson JE et al (2000) Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Mol Ecol 9:421–431

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Weber JL, May PE (1989) Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet 44:388–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • West RG (1967) The quaternary of the British Isles. The geologic systems. In: Rankama K (ed) The Quaternary, vol 2, pp 1–87. Interscience, New York

    Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Yensen E, Tarifa T (2003) Galictis cuja. Mammal Spec 728:1–8

    Article  Google Scholar 

  • Yerena E (1998) Protected areas for the Andean bear in South America. Ursus 10:101–106

    Google Scholar 

  • Yerena E, Monsalve Dam D, Torres D, Sánchez A, García-Rangel S, Bracho A, Martínez Z, Gómez I (2007) Plan de Acción para la Conservación del Oso Andino (Tremarctos ornatus) en Venezuela (2006–2016). Fundación Andígena, FUDENA, Universidad Simón Bolívar, Mérida, Venezuela, Mérida, Venezuela

    Google Scholar 

  • Yu L, Li QW, Ryder OA, Zhang YP (2004) Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes. Mol Phylogenet Evol 32:480–494

    Article  CAS  PubMed  Google Scholar 

  • Zhang YP, Ryder OA (1993) Mitochondrial DNA sequence evolution in the Arctoidea. Proc Natl Acad Sci USA 90:9557–9561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YP, Ryder OA (1994) Phylogenetic relationships of bears (the ursidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 3:351–359

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to express their gratitude to collaborators who have obtained samples directly from wild: Andrés Eloy Bracho, Isaac Goldstein (Venezuela), Leonardo Arias (Ecuador), Hector Restrepo, Sergio Sandoval, Daniel Rodríguez, Pedro Moreno (Colombia), Heinz Pflenge, Hugo Gálvez, Judith Figueroa (Peru), Robert Wallace, Susan Paisley, and Virginia Ossio (Bolivia). We are indebted to the Academic Vicerrectory of the Pontificia Universidad Javeriana at Bogotá (Colombia) and to Corponariño (Aida Delgado, Diana Ocaña Saltikova) at Pasto (Nariño, Colombia) for providing monetary resources to carry out this research. Also we are grateful to Instituto von Humboldt (Colombia), Ministerio del Ambiente Ecuatoriano (MAE; Ecuador), Consejo Nacional del Ambiente and the Instituto Nacional de Recursos Naturales (INRENA; Peru), and Colección Boliviana de Fauna and CITES (Bolivia) for their role in facilitating the obtainment of the collection permits.

Compliance with ethical standards

Conflict of interest The authors confirm that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratorio de Genética de Poblaciones Molecular–Biología Evolutiva. Unidad de Genética, Departamento de Biología. Facultad de Ciencias, Pontificia Universidad Javeriana, Cra 7A no 43-82, Bogotá, DC, Colombia

    Manuel Ruiz-García & Jessica Yanina Arias Vásquez

  2. Instituto Nacional de Biodiversidad (INABIO), Pje Rumipamba N.341 y Av. De los Shyris, 170135, Quito, Ecuador

    Manuel Ruiz-García & Armando Castellanos

  3. Andean Bear Foundation, La Isla, Quito, Ecuador

    Armando Castellanos

  4. AG Zoologischer Garten Köln (Kölner zoo), Riehler Straße 173, 50735, Cologne, Germany

    Lydia Kolter

  5. Math, Science and Technology Department, University of Minnesota Crookston, 2900 University Ave, Crookston, MN, 56716, USA

    Joseph M. Shostell

Authors
  1. Manuel Ruiz-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica Yanina Arias Vásquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Armando Castellanos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lydia Kolter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph M. Shostell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Ruiz-García .

Editor information

Editors and Affiliations

  1. Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, Mexico

    Jorge Ortega

  2. Center for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    Jesus E. Maldonado

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Smithsonian Institution

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ruiz-García, M., Vásquez, J.Y.A., Castellanos, A., Kolter, L., Shostell, J.M. (2020). Molecular Evolution (Mitochondrial and Nuclear Microsatellites Markers) in the Andean Bear (Tremarctos ornatus; Ursidae, Carnivora): How Many ESUs Are There?. In: Ortega, J., Maldonado, J. (eds) Conservation Genetics in Mammals. Springer, Cham. https://doi.org/10.1007/978-3-030-33334-8_8

Download citation

Publish with us

Policies and ethics

Search

Navigation