Advertisement

Conservation Genetics

, Volume 15, Issue 3, pp 631–653 | Cite as

Phylogeography and population history of Leopardus guigna, the smallest American felid

  • Constanza Napolitano
  • Warren E. Johnson
  • Jim Sanderson
  • Stephen J. O’Brien
  • A. Rus Hoelzel
  • Rachel Freer
  • Nigel Dunstone
  • Kermit Ritland
  • Carol E. Ritland
  • Elie Poulin
Research Article

Abstract

The guigna (Leopardus guigna) is the smallest and most-restricted New World cat species, inhabiting only around 160,000 km2 of temperate rain forests in southern South America and is currently threatened by habitat loss, fragmentation and human persecution. We investigated phylogeographic patterns of genetic diversity, demographic history and barriers to gene flow with 116 individuals sampled across the species geographic range by analyzing 1,798 base pairs of the mtDNA (496 bp HVSI region, 720 bp NADH-5 gene, 364 bp from 16S gene and 218 bp from ATP-8 gene) and 15 microsatellite loci. Mitochondrial DNA data revealed a clear phylogeographic pattern with moderate separation between northern and southern Chilean populations supporting recognized subspecific partitions based on morphology. A recent demographic expansion was inferred for the southern-most group (San Rafael Lake), presumably due to the complete coverage of this area during the last glacial period, 28000–16000 years BP. Geographical barriers such as the Andes Mountains and the Chacao Channel have partially restricted historic and more-recent gene flow and the Chiloé Island population has diverged genetically since being separated from the mainland 7000 years BP. This is the first study of the genetic structure of this threatened species throughout its whole geographic range.

Keywords

Leopardus guigna Felid Phylogeography Demographic history Dispersal barriers 

Notes

Acknowledgments

Guignas were captured with permission from the Agriculture and Livestock Service (SAG) in Chile, capture permit numbers 814/13-Feb-2008, 109/9-Jan-2009, 1220/22-Feb-2010 and 1708/26-Mar-2010. Samples were obtained in Argentina with permission from the National Parks Administration (APN), permit number 1002/8-May-2009. Samples were imported with permission from the Agriculture and Livestock Service (SAG) in Chile, permit number 30/09. C.N. acknowledges support from the doctoral fellowship ICM P05-002 from the Instituto de Ecología y Biodiversidad (IEB, Facultad de Ciencias, Universidad de Chile), the Emerging Leaders in The Americas Program (ELAP, Canadian Bureau for International Education, Government of Canada) and Becas Chile para pasantías doctorales 2010 (CONICYT, Chile). This study was funded by the Instituto de Ecología y Biodiversidad (Facultad de Ciencias, Universidad de Chile), Panthera Kaplan Awards Program (Panthera Foundation, New York, USA), Scott Neotropical Fund Award (Cleveland Metroparks Zoo & the Cleveland Zoological Society, Cleveland, USA) and the Eric York Scholarship (Felidae Conservation Fund, California, USA). This research was supported in part by the Intramural Research Program of the NCI, NIH. We wish to thank Benito González, Emma Elgueta, Milton Gallardo (Universidad Austral), Jaime Rau (Universidad de Los Lagos), Oscar Skewes (Universidad de Concepción), Bárbara Zentilli (CODEFF), Denise Donoso, Nicolás Gálvez, Felipe Hernández, Elke Schüttler, Cristián Bonacic, Martín Monteverde (Centro de Ecología Aplicada del Neuquén—Argentina), José Luis Brito (Museo Municipal de Ciencias Naturales y Arqueología de San Antonio), Juan Carlos Torres (Museo de Historia Natural Santiago), José Yáñez (Museo de Historia Natural Santiago), Osvaldo Rojas (Museo de Historia Natural Calama), Fernando Soto (Museo de Historia Natural de Valparaíso), Elvira Solar (Museo de Zoología Universidad de Concepción), Franklin Troncoso (Museo de Historia Natural de Concepción), Luis Villanueva (SAG VII Región), Cecilia González (SAG RM), David Flores (Museo de Ciencias Naturales Bernardino Rivadavia—Argentina), Diego Verzi (Museo de La Plata—Argentina), Manuel Valdés (Parque Tantauco), Bernardita Silva, Lito Quezada, Maximiliano Sepúlveda, Javier Cabello, Alejandro Bravo (Universidad Austral), Jorge Valenzuela (CECPAN), Andrés Charrier, Juan Luis Celis, Buin Zoo and Fidel Ovidio Castro (Banco de Recursos Genéticos, Facultad de Ciencias Veterinarias, Universidad de Concepción, Campus Chillán) for generous collaboration with samples for this study. We specially thank Magdalena Bennett for map elaboration. We thank Sylvain Faugeron and Juliana Vianna de Abreu for help with molecular markers. Special thanks to Jennifer Hetz, Mónica Mora, Valentina Sánchez, Tatiana Vuskovic, Verónica Solé, Rousset Palou, Yuri Zúñiga and Juan Vidal for assisting in the capture of guignas. We thank Raleigh International for logistical support in collection of samples at San Rafael Lake. We thank Parque Ahuenco, especially to Alberto Carvacho, for kindly letting us work in their lands. We thank the Sindicato de Pescadores Mar Adentro from Chepu, especially to Carlos Villarroel, for their kind help during field work. We thank Parque Tantauco, especially to Alan Bannister, for their kind support and for letting us work in their lands. We thank the Senda Darwin Foundation, Inés Hanning from Caulín, and many other local land owners in Chiloé Island who kindly let us work in their lands.

Supplementary material

10592_2014_566_MOESM1_ESM.docx (566 kb)
Supplementary material 1 (DOCX 565 kb)

References

  1. Abraham EM, Garleff K, Liebricht H et al (2000) Geomorphology and Paleoecology of the Arid Diagonal in southern South America. Zeitschrift für Angewandte Geologie SH1:55–61Google Scholar
  2. Acosta-Jamett G, Simonetti JA (2004) Habitat use by Oncifelis guigna and Pseudalopex culpaeus in a fragmented forest landscape in central Chile. Biodivers Conserv 13:1135–1151Google Scholar
  3. Acosta-Jamett G, Simonetti JA, Bustamante RO et al (2003) Metapopulation approach to assess survival of Oncifelis guigna in fragmented forests of central Chile: a theoretical model. J Neotrop Mammal 10:217–229Google Scholar
  4. Aragón E, Goin FJ, Aguilera YE et al (2011) Palaeogeography and palaeoenvironments of northern Patagonia from the Late Cretaceous to the Miocene: the Palaeogene Andean gap and the rise of the North Patagonian High Plateau. Biol J Linn Soc 103:305–315Google Scholar
  5. Armesto JJ, León-Lobos P, Arroyo MTK (1996) Los bosques templados de Chile y Argentina: una isla biogeográfica. In: Armesto JJ, Villagrán C, Arroyo MTK (eds) Ecología de los bosques nativos de Chile. Editorial Universitaria, Santiago, pp 23–28Google Scholar
  6. Arroyo MTK, Cavieres L, Peñaloza A et al (1996) Relaciones fitogeográficas y patrones regionales de riqueza de especies en la flora del bosque lluvioso templado de Sudamérica. In: Armesto JJ, Villagrán C, Arroyo MTK (eds) Ecología de los bosques nativos de Chile. Editorial Universitaria, Santiago, pp 71–99Google Scholar
  7. Arroyo MTK, Marquet PA, Marticorena C et al (2004) Chilean winter rainfall-Valdivian forests. In: Mittermeier RA, Gil PR, Hoffmann M et al (eds) Hotspots Revisited: Earth’s Biologically Wealthiest and most Threatened Ecosystems. CEMEX, México D.F., pp 99–103Google Scholar
  8. Balding DJ (2003) Likelihood-based inference for genetic correlation coefficients. Theor Popul Biol 63:221–230PubMedGoogle Scholar
  9. Bandelt H-J, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  10. Bellemain E, Taberlet P (2004) Improved noninvasive genotyping method: application to brown bears (Ursus arctos) feces. Mol Ecol Notes 4:519–522Google Scholar
  11. Belmar-Lucero S, Godoy P, Ferrés M et al. (2009) Range expansion of Oligoryzomys longicaudatus (Rodentia, Sigmodontinae) in Patagonian Chile, and first record of Hantavirus in the region. Rev Chil Hist Nat 82:265-–275Google Scholar
  12. Bennett KD (2004) Continuing the debate on the role of Quaternary environmental change for macroevolution. Philos Trans R Soc Lond B 359:295–303Google Scholar
  13. Bennett KD, Provan J (2008) What do we mean by refugia? Quat Sci Rev 27:2449-–2455Google Scholar
  14. Bermingham E, Moritz C (1998) Comparative phylogeography: concepts and applications. Mol Ecol 7:367–369Google Scholar
  15. Bonin A, Bellemain E, Bronken Eidesen P et al (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273PubMedGoogle Scholar
  16. Bosshard M (2011) Evidencias genéticas de la historia glacial de Laureliopsis philippiana. Dissertation, Universidad de Chile, Santiago, Chile. p 33Google Scholar
  17. Burban C, Petit RJ, Carcreff E et al (1999) Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Mol Ecol 8:1593–1602PubMedGoogle Scholar
  18. Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54:2107–2118PubMedGoogle Scholar
  19. Cabrera A (1957) Catálogo de los mamíferos de América del Sur. Parte 1, Metatheria-Unguiculata-Carnivora. Revista del Museo Argentino de Ciencias Naturales 4:1–37Google Scholar
  20. Clapperton CM (1993) Nature of environmental changes in South America at the Last Glacial Maximum. Palaeogeogr Palaeoclim Palaeoecol 101:189–208Google Scholar
  21. Cofre H, Marquet PA (1999) Conservation status, rarity, and geographic priorities for conservation of Chilean mammals: an assessment. Biol Conserv 88:53–68Google Scholar
  22. CONAMA (2011) Reglamento para la Clasificación de las Especies Silvestres. Séptimo proceso para la clasificación de especies Acuerdo N°9/2011. Ministerio Secretaría General de la Presidencia de la República de ChileGoogle Scholar
  23. Correa P, Roa A (2005) Relaciones tróficas entre Oncifelis guigna, Lycalopex culpaeus, Lycalopex griseus y Tyto alba en un ambiente fragmentado de la zona central de Chile. J Neotrop Mammal 12:57–60Google Scholar
  24. Cossios D, Lucherini M, Ruiz-García M et al (2009) Influence of ancient glacial periods on the Andean fauna: the case of the pampas cat (Leopardus colocolo). BMC Evol Biol 9:1–12Google Scholar
  25. Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. TREE 15:290–295PubMedGoogle Scholar
  26. Creel S, Spong G, Sands J et al (2003) Population size estimation in Yellowstone wolves with errorprone noninvasive microsatellite genotypes. Mol Ecol 12:2003–2009PubMedGoogle Scholar
  27. Culver M, Johnson WE, Pecon-Slattery J et al (2000) Genomic ancestry of the American puma (Puma concolor). J of Heredity 91:186–197Google Scholar
  28. Dalén L, Nyström V, Valdiosera C et al (2007) Ancient DNA reveals lack of postglacial habitat tracking in the arctic fox. Proc Natl Acad Sci USA 104:6726–6729PubMedCentralPubMedGoogle Scholar
  29. Denton GH, Heusser CJ, Lowell TV et al (1999) Interhemispheric linkage of paleoclimate during the last glaciation. Geogr Ann 81:107–153Google Scholar
  30. Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. Proc R Soc B 275:2743–2748PubMedCentralPubMedGoogle Scholar
  31. Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCentralPubMedGoogle Scholar
  32. Dunstone N, Durbin L, Wyllie I, Freer RA, Acosta JG, Mazzolli M, Rose S (2002) Spatial organization, ranging behaviour and habitat use of the kodkod (Oncifelis guigna) in southern Chile. J Zool 257:1–11Google Scholar
  33. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581PubMedGoogle Scholar
  34. Eizirik E, Bonatto SL, Johnson WE et al (1998) Phylogeographic patterns and evolution of the mitochondrial DNA control region in two Neotropical cats (Mammalia, Felidae). J Mol Evol 47:613–624PubMedGoogle Scholar
  35. Eizirik E, Kim J-H, Menotti-Raymond M et al (2001) Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol Ecol 10:65–79PubMedGoogle Scholar
  36. Eronen JT, Rook L (2004) The Mio-Pliocene European primate fossil record: dynamics and habitat tracking. J Hum Evol 47:323–341PubMedGoogle Scholar
  37. 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 Res 10:564–567Google Scholar
  38. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  39. Filatov DA (2002) Proseq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624Google Scholar
  40. Formas JR, Brieva LM (2000) Population genetics of the Chilean frog Batrachyla leptopus (Leptodactylidae). Genet Mol Biol 23:43–48Google Scholar
  41. Frankham R, Ballou JD, Briscoe DA (2005) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 617Google Scholar
  42. Frantz AC, Pope LC, Carpenter PJ et al (2003) Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Mol Ecol 12:1649–1661PubMedGoogle Scholar
  43. Freeman AR, Machugh DE, Mckeown S et al (2001) Sequence variation in the mitochondrial DNA control region of wild African cheetahs (Acinonyx jubatus). Heredity 86:355–362PubMedGoogle Scholar
  44. Freer RA (2004) The Spatial Ecology of the Güiña (Oncifelis guigna) in Southern Chile. D.Phil. Dissertation. University of Durham, UK. p 219Google Scholar
  45. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  46. Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedCentralPubMedGoogle Scholar
  47. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, Causes, and Consequences, with Insights from Animal Mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423Google Scholar
  48. Gajardo R (1994) La vegetación natural de Chile: Clasificación y distribución geográfica. Editorial Universitaria, ChileGoogle Scholar
  49. Gálvez N, Hernández F, Laker J et al (2013) Forest cover outside protected areas plays an important role in the conservation of the Vulnerable guiña Leopardus guigna. Oryx 47:251–258Google Scholar
  50. Garzione CN, Hoke GD, Libarkin JC et al (2008) Rise of the Andes. Science 320:1304–1307PubMedGoogle Scholar
  51. Graham CH, VanDerWal J, Phillips SJ et al. (2010) Dynamic refugia and species resistence: Tracking spatial shifts in habitat trough time. Ecography 33:1062-–1069Google Scholar
  52. Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715Google Scholar
  53. Haig SM, Wagner RS, Forsman ED et al (2001) Geographic variation and genetic structure in Spotted Owls. Conserv Genet 2:25–40Google Scholar
  54. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9Google Scholar
  55. Hanski I, Simberloff D (1997) The metapopulation approach, its history, conceptual domain, and application to conservation. In: Hanski IA, Gilpin ME (eds) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San Diego, pp 5–26Google Scholar
  56. Hanski I, Pöyry J, Pakkala T et al (1995) Multiple equilibria in metapopulation dynamics. Nature 377:618–621Google Scholar
  57. Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on bayesian skyline plot inferences of demographic history. PLoS ONE 8(5):e62992PubMedCentralPubMedGoogle Scholar
  58. Herrmann TM, Schüttler E, Benavides P et al (2013) Values, animal symbolism, and human-animal relationships associated to two threatened felids in Mapuche and Chilean local narratives. J Ethnobiol Ethnomed 9:41–56PubMedCentralPubMedGoogle Scholar
  59. Heusser CJ, Heusser LE, Lowell TV (1999) Paleoecology of The Southern Chilean Lake District-Isla Grande de Chiloé during Middle-late Llanquihue Glaciation and Deglaciation. Geogr Ann Phys Geogr 81:231–284Google Scholar
  60. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans Roy Soc Lond B 359:183–195Google Scholar
  61. Himes CMT, Gallardo MH, Kenagyg J (2008) Historical biogeography and postglacial recolonization of South American temperate rain forest by the relictual marsupial Dromiciops gliroides. J Biogeog 35:1415–1424Google Scholar
  62. Hinojosa LF, Villagrán C (1997) Historia de los bosques del sur de América, I: antecedentes paleobotánicos, geológicos y climáticos del Terciario del Cono Sur de América. Rev Chil Hist Nat 70:225–239Google Scholar
  63. Ho SYW, Shapiro B (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11:423–434PubMedGoogle Scholar
  64. Hoelzel AR, Green A (1992) Analysis of population-level variation by sequencing PCR-amplified DNA. In: Hoelzel AR (ed) Molecular genetic analysis of populations. Oxford University Press, Oxford, pp 159–187Google Scholar
  65. Hofreiter M, Stewart J (2009) Ecological change, range fluctuations and population dynamics during the Pleistocene. Curr Biol 19:R584–R594PubMedGoogle Scholar
  66. Huelsenbeck JP, Bull JJ, Cunningham CW (1996) Combining data in phylogenetic analysis. TREE 11:152–158PubMedGoogle Scholar
  67. Ihaka R, Gentleman R (1996) R: a language for data analysis and Graphics. J Comput Graphical Statistics 5:299–314Google Scholar
  68. Inskip C, Zimmermann A (2009) Human-felid conflict: a review of patterns and priorities worldwide. Oryx 43:18–34Google Scholar
  69. IUCN (2013) IUCN Red List of Threatened Species. Version 2013.2. <www.iucnredlist.org>. Accessed 29 Nov 2013
  70. Johnson WE, Culver M, Iriarte AJ et al (1998) Tracking the evolution of the elusive Andean Mountain Cat (Oreailurus jacobita) from mitochondrial DNA. J Hered 89:227–232PubMedGoogle Scholar
  71. Johnson WE, Pecon-Slattery J, Eizirik E et al (1999) Disparate phylogeographic patterns of molecular genetic variation in four closely related South American small cat species. Mol Ecol 8:S79–S94PubMedGoogle Scholar
  72. Johnson WE, Eizirik E, Murphy WJ et al (2006) The Late Miocene radiation of modern Felidae: a genetic assessment. Science 311:73–77PubMedGoogle Scholar
  73. Klicka J, Zink RM (1997) The importance of recent ice ages in speciation: a failed paradigm. Science 277:1666–1669Google Scholar
  74. Kottek M, Grieser J, Beck C et al (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263Google Scholar
  75. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770PubMedGoogle Scholar
  76. Lessa EP, D’Elia G, Pardiñas UFJ (2010) Genetic footprints of late Quaternary climate change in the diversity of Patagonian-Fueguian rodents. Mol Ecol 19:3031–3037PubMedGoogle Scholar
  77. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedGoogle Scholar
  78. Lindenmayer DB, Fischer J (2006) Habitat Fragmentation and Landscape Change: An Ecological and Conservation Synthesis. Island Press, WashingtonGoogle Scholar
  79. Malcolm JR, Liu C, Neilson RP et al (2005) Global warming and extinctions of endemic species from biodiversity hotspots. Conserv Biol 20:538–548Google Scholar
  80. Mathiasen P, Premoli AC (2010) Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America. Mol Ecol 19:371–385PubMedGoogle Scholar
  81. McCulloch RD, Bentley MJ, Purves RS et al (2000) Climatic inferences from glacial and palaeoecological evidence at the last glacial termination, southern South America. J Quat Sci 15:409–417Google Scholar
  82. Menotti-Raymond M, David VA, Lyons LA et al (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23PubMedGoogle Scholar
  83. Mercer JH (1983) Cenozoic glaciation in the Southern Hemisphere. Annu Rev Earth Planet Sci 11:99–132Google Scholar
  84. Miller MP (2005) Alleles In Space: computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724PubMedGoogle Scholar
  85. Miller MP, Haig SM, Wagner RS (2006) Phylogeography and spatial genetic structure of the Southern Torrent Salamander: implications for conservation and management. J Hered 97:561–570PubMedGoogle Scholar
  86. Montenegro PN (2011) Filogeografía de Weinmannia trichosperma: Herencia genética de una historia glacial en el sur de Sudamérica. Dissertation, Universidad De Chile. pp 52Google Scholar
  87. Moreno PI (2000) Climate, fire, and vegetation between about 13000 and 9200 14C yr B.P. in the Chilean Lake District. Quat Res 54:81–89Google Scholar
  88. Moreno PI, Villagrán C, Marquet PA et al (1994) Quaternary paleobiogeography of northern and central Chile. Rev Chil Hist Nat 67:487–502Google Scholar
  89. Moreno PI, Lowell TV, Jacobson JR Jr et al (1999) Abrupt vegetation and climate changes during the last glacial maximum and last termination in the Chilean Lake District: a case study from Canal de la Puntilla (41°S). Geogr Ann 81:285–311Google Scholar
  90. Moritz C (2002) Strategies to protect biological diversity and the processes that sustain it. Systematic Biol 51:238–254Google Scholar
  91. Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedGoogle Scholar
  92. Napolitano C (2012). Filogeografía, inferencia demográfica y genética de la conservación del felino Leopardus guigna en el sur de Sudamérica. Dissertation, Universidad de Chile. pp 255Google Scholar
  93. Navidi W, Arnheim N, Waterman MS (1992) A multiple-tube approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. Am J Hum Genet 50:347–359PubMedCentralPubMedGoogle Scholar
  94. Nicholson GA, Smith V, Jónsson F et al (2002) Assessing population differentiation and isolation from single nucleotide polymorphism data. J R Stat Soc B 64:695–715Google Scholar
  95. Nowell K, Jackson P (1996) Status survey and conservation action plan: wild cats. IUCN/SSC Cat Specialist Group, GlandGoogle Scholar
  96. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  97. Olson DM, Dinerstein E, Wikramanayake ED et al (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933–938Google Scholar
  98. Osgood WH (1943) The mammals of Chile. Field Mus Nat Hist Zool 30:1–268Google Scholar
  99. Palma RE, Rivera-Milla E, Yates TL et al (2002) Phylogenetic and biogeographic relationships of the mouse opossum Thylamys (Didelphimorphia, Didelphidae) in southern South America. Mol Phylogenet Evol 25:245–253Google Scholar
  100. Palma RE, Rivera-Milla E, Salazar-Bravo J et al (2005) Phylogeography of Oligoryzomys longicaudatus (Rodentia: sigmodontinae) in temperate South America. J Mammal 86:191–200Google Scholar
  101. Palsbøll PJ, Bérubé M, Allendorf FW (2006) Identification of management units using population genetic data. TREE 22:11–16PubMedGoogle Scholar
  102. Pardiñas UFJ, Teta P, D’Elía G et al (2011) The evolutionary history of sigmodontine rodents in Patagonia and Tierra del Fuego. Biol J Linn Soc 103:495–513Google Scholar
  103. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Rev Ecol Evol Syst 2006(37):637–669Google Scholar
  104. Patterson BD (2010) Climate change and faunal dynamics in the uttermost part of the earth. Mol Ecol 19:3019–3021PubMedGoogle Scholar
  105. Peter MB, Wegmann D, Excoffier L (2010) Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol Ecol 19:4648–4660PubMedGoogle Scholar
  106. Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology? Proc Royal Soc B 273:1049–1053Google Scholar
  107. Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity. I: haploid locus. Theor Appl Genet 90:462–470PubMedGoogle Scholar
  108. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245PubMedCentralPubMedGoogle Scholar
  109. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  110. Quintana V, Yáñez J, Valdebenito M (2000) Orden Carnivora. In: Muñoz A, Yáñez J (eds) Mamíferos de Chile. CEA Ediciones, Valdivia, pp 155–187Google Scholar
  111. Raymond R, Rousset M (1995) GENEPOP: (Version 4) population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  112. Reside AE, VanDerWal J, Phillips BL et al (2013) Climate change refugia for terrestrial biodiversity: defining areas that promote species persistence and ecosystem resilience in the face of global climate change. National Climate Change Adaptation Research Facility, Gold Coast, p 216Google Scholar
  113. Rodríguez-Serrano E, Cancino RA, Palma RE (2006) Molecular phylogeography of Abrothrix olivaceus (Rodentia: Sigmodontinae) in Chile. J Mammal 87:971–-980Google Scholar
  114. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  115. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106Google Scholar
  116. Ruiz-García M, Luengos E, Lucherini M et al (2001) Distribución alélica para los microsatélites FCA96, FCA45, FCA43, FCA08, FCA126 para los félidos neotropicales Oncifelis geoffroyi, Oncifelis guigna y Lynchailurus colocolo en Argentina, Paraguay y Bolivia: Intento de diferenciación de especies mediante excrementos y pelos. Acta Biol Colomb 6:79Google Scholar
  117. Saiki RK, Scharf S, Faloona F et al (1985) Enzimatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350PubMedGoogle Scholar
  118. Samaniego H, Marquet PA (2009) Mammal and butterfly species richness in Chile: taxonomic covariation and history. Rev Chil Hist Nat 82:135–151Google Scholar
  119. Sandel B, Arge L, Dalsgaard B et al (2011) The influence of Late Quaternary climate-change velocity on species endemism. Science 334:660–664PubMedGoogle Scholar
  120. Sanderson J, Sunquist ME, Iriarte A (2002) Natural history and landscape-use of guignas (Oncifelis guigna) on Isla Grande de Chiloé, Chile. J Mammal 83:608–613Google Scholar
  121. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotech 18:233–234Google Scholar
  122. Segovia RA, Pérez MF, Hinojosa LF (2012) Genetic evidence for glacial refugia of the temperate tree Eucryphia cordifolia (Cunoniaceae) in Southern South America. Am J Bot 99:121–129PubMedGoogle Scholar
  123. Sérsic AN, Cosacov A, Cocucci AA et al (2011) Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biol J Linn Soc Lond 103:475–494Google Scholar
  124. Sillero-Zubiri C, Laurenson MK (2001) Interactions between carnivores and local communities: conflict or co-existence? In: Gittleman JL, Funk SM, Macdonald D, Wayne RK (eds) Carnivore Conservation. Cambridge University Press, Cambridge, pp 282–312Google Scholar
  125. Silva-Rodriguez EA, Ortega-Solís GR, Jiménez JE (2007) Human attitudes toward wild felids in a human-dominated landscape of Southern Chile. Cat News 46:19–21Google Scholar
  126. Simonetti JA, Acosta G (2002) Conservando biodiversidad en tierras privadas: el ejemplo de los carnívoros. Ambiente y Desarrollo 18:51–59Google Scholar
  127. Sinclair EA, Swenson EL, Wolfe ML et al (2001) Gene flow estimates in Utah’s cougars imply management beyond Utah. Anim Conserv 4:257–264Google Scholar
  128. Smith MF, Kelt DA, Patton JL (2001) Testing models of diversification in mice in the Abrothrix olivaceus/xanthorhinus complex in Chile and Argentina. Mol Ecol 10:397–405PubMedGoogle Scholar
  129. Smith DA, Ralls K, Hurt A et al (2006) Assessing reliability of microsatellite genotypes from kit fox faecal samples using genetic and GIS analyses. Mol Ecol 15:387–406PubMedGoogle Scholar
  130. Taberlet P, Griffin S, Goossens B et al (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194PubMedCentralPubMedGoogle Scholar
  131. Stewart JR (2008) The progressive effect of the individualistic response of species to Quaternary climate change: an analysis of British mammalian faunas. Quat Sci Rev 27:2499-–2508Google Scholar
  132. Stewart JR (2009) The evolutionary consequence of the individualistic response to climate change. J Evol Biol 22:2363-–2375Google Scholar
  133. Taberlet P, Fumagalli L, Wust-Saucy A-G et al (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464PubMedGoogle Scholar
  134. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327PubMedGoogle Scholar
  135. Tajima F (1989) Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. Genetics 123:585–595PubMedCentralPubMedGoogle Scholar
  136. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedGoogle Scholar
  137. Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16PubMedGoogle Scholar
  138. Taylor PD, Fahrig L, Henein K et al (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573Google Scholar
  139. Trigo TC, Freitas TRO, Kunzler G et al (2008) Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol Ecol 17:4317–4333PubMedGoogle Scholar
  140. Uphyrkina O, Johnson WE, Quigley H et al (2001) Phylogenetics, genome diversity and origin of modern leopard, Panthera pardus. Mol Ecol 10:2617–2633PubMedGoogle Scholar
  141. Van Oosterhout C, Hutchinson WF, Wills DPM et al (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538Google Scholar
  142. Victoriano PF, Ortíz JC, Benavides ER et al (2008) Comparative phylogeography of codistributed species of Chilean Liolaemus (Squamata: Tropiduridae) from the central-southern Andean range. Mol Ecol 17:2397–2416PubMedGoogle Scholar
  143. Vidal MA, Moreno PI, Poulin E (2012) Genetic diversity and insular colonization of Liolaemus pictus (Squamata, Liolaeminae) in north-western Patagonia. Aust Ecol 37:67–77Google Scholar
  144. Villagrán C (1988) Expansion of Magellanic Moorland during the late Pleistocene: palynological evidence from northern Isla de Chiloé, Chile. Quat Res 30:304–314Google Scholar
  145. Villagrán C, Hinojosa LF (1997) Historia de los bosques del sur de Sudamérica, II: análisis fitogeográfico. Rev Chil Hist Nat 70:241–267Google Scholar
  146. Villagrán C, Hinojosa LF (2005) Esquema Biogeográfico de Chile. In: Morrone JJ, Llorente Bousquets J (eds) Regionalización Biogeográfica en Iberoámeríca y tópicos afines. Ediciones de la Universidad Nacional Autónoma de México, Jiménez Editores, México, pp 551–577Google Scholar
  147. Villagrán C, Armesto JJ, Leiva R (1986) Recolonización postglacial de Chiloé insular: evidencias basadas en la distribución geográfica y los modos de dispersión de la flora. Rev Chil Hist Nat 59:19–39Google Scholar
  148. Waits LP, Paetkau D, Strobeck C (1998) The genetics of the bears of the world. In: Servheen C (ed) Bear Conservation Act. IUCN, Gland, pp 25–32Google Scholar
  149. Wayne RK, Lehman N, Allard MW et al (1992) Mitochondrial DNA variability of the gray wolf: genetic consequences of population decline and habitat fragmentation. Conserv Biol 6:559–569Google Scholar
  150. Webb SD (1991) Ecogeography and the great American interchange. Paleobiology 17:266–280Google Scholar
  151. Willson K, Newton A, Echeverría C et al (2005) A vulnerability analysis of the temperate forests of south central Chile. Biol Conserv 122:9–21Google Scholar
  152. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedCentralPubMedGoogle Scholar
  153. Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of wildlife inside protected areas. Science 280:2126–2128PubMedGoogle Scholar
  154. Woodroffe R, Thirgood S, Rabinowitz A (2005) People and wildlife: conflict or coexistence?. Cambridge University Press, UKGoogle Scholar
  155. Wozencraft WC (1993) Order Carnivora. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference. Smithsonian Institution Press, Washington, DC, pp 279–348Google Scholar
  156. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564Google Scholar
  157. Zorondo F (2005) Conservación de carnívoros en Chile central: el factor social. Thesis, Facultad de Ciencias, Universidad de Chile, Santiago, Chile. pp 41Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Constanza Napolitano
    • 1
  • Warren E. Johnson
    • 2
    • 9
  • Jim Sanderson
    • 3
  • Stephen J. O’Brien
    • 4
  • A. Rus Hoelzel
    • 5
  • Rachel Freer
    • 5
    • 6
  • Nigel Dunstone
    • 5
    • 7
  • Kermit Ritland
    • 8
  • Carol E. Ritland
    • 8
  • Elie Poulin
    • 1
  1. 1.Laboratorio de Ecología Molecular & Instituto de Ecología y Biodiversidad, Departamento de Ciencias Ecológicas, Facultad de CienciasUniversidad de ChileSantiagoChile
  2. 2.Laboratory of Genomic DiversityNational Cancer InstituteFrederickUSA
  3. 3.Small Wild Cat Conservation FoundationCampbellUSA
  4. 4.Theodosius Dobzhansky Center for Genome BioinformaticsSt. Petersburg State UniversitySt. PetersburgRussia
  5. 5.School of Biological and Biomedical SciencesDurham UniversityDurhamUK
  6. 6.FPCR Environment & Design Ltd.LockingtonUK
  7. 7.Natural History New ZealandDunedinNew Zealand
  8. 8.Department of Forest and Conservation SciencesUniversity of British ColumbiaVancouverCanada
  9. 9.Smithsonian Conservation Biology InstituteNational Zoological ParkFront RoyalUSA

Personalised recommendations