Ancient DNA evidence of prolonged population persistence with negligible genetic diversity in an endemic tuco-tuco (Ctenomys sociabilis)

Journal of Mammalogy

Volumn 84, Issue 2, 2003, Pages 403-417

  Hadly, Elizabeth A ^a   Van Tuinen, Marcel ^a   Chan, Yvonne ^a   Heiman, Kimberly ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

aDNA; Climatic change; Endemism; Holocene; Patagonia; Population bottleneck

Indexed keywords

CLIMATE CHANGE; DISTURBANCE; GENETIC VARIATION; PALEOECOLOGY; POPULATION BOTTLENECK; POPULATION GENETICS; RODENT;

ARGENTINA;

CTENOMYS; CTENOMYS HAIGI; CTENOMYS MAULINUS; CTENOMYS SOCIABILIS; RAPTORES; RODENTIA;

EID: 0037565013     PISSN: 00222372     EISSN: None     Source Type: Journal    
DOI: 10.1644/1545-1542(2003)084<0403:ADEOPP>2.0.CO;2     Document Type: Article

References (88)

1. AAGESEN, D. 2000. Crisis and conservation at the end of the world: sheep ranching in Argentine Patagonia. Environmental Conservation 27:208-215.
2. AMOS, W. 1999. Problems with the measurement of genetic diversity and genetic distance. Pp. 75-100 in Genetics and the extinction of species (L. F. Landweber and A. P. Dobson, eds.). Princeton University Press, Princeton, New Jersey.
3. BARNES, I., P. MATHEUS, B. SHAPIRO, D. JENSEN, AND A. COOPER. 2002. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science 295:2267-2270.
4. BARNOSKY, A. D., E. A. HADLY, AND C. J. BELL. 2003. Mammalian response to global warming on varied temporal scales. Journal of Mammalogy 84:354-368.
5. BIANCHI, M. M., J. MASSAFERRO, G. R. ROSS, A. J. AMOS, AND A. LAMI. 1999. Late Pleistocene and early Holocene ecological response of Lake El Trébol (Patagonia, Argentina) to environmental changes. Journal of Paleolimnology 22:137-148.
6. BOOM, R., C. J. A. SOL, M. M. M. SALIMANS, C. L. JANSEN, P. M. E. WERTHEIM-VAN DILLEN, AND J. VAN DER NOORDAA. 1990. Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28:495-503.
7. BOUZAT, J. I., H. H. CHENG, H. A. LEWIN, R. L. WESTEMEIER, J. D. BRAWN, AND K. N. PAIGE. 1998. Genetic evaluation of a demographic bottleneck in the greater prairie chicken. Conservation Biology 12:836-843.
8. BRADLEY, R. D., AND R. J. BAKER. 2001. A test of the genetic species concept: cytochrome-b sequences and mammals. Journal of Mammalogy 82:960-973.
9. BROECKER, W. 2001. Was the Medieval Warm Period global? Science 291:1497-1499.
10. CAMERON, G. N. 2000. Community ecology of subterranean rodents. Pp. 227-256 in Life underground: the biology of subterranean rodents (E. A. Lacey, J. L. Patton, and G. N. Cameron, eds.). University of Chicago Press, Chicago, Illinois.
11. CHRISTIE, M. I. (COORD.). 1984. Informe preliminar del relevamiento de fauna de los Parques Nacionales Lanin y Nahuel Haupi. Mamiferos. Parques Nacionales-INVAP, San Carlos de Bariloche, Argentina 3.
12. COMPARATORE, V. M., M. AGNUSDEL, AND C. BUSCH. 1992. Habitat relations in sympatric populations of Ctenomys australis and Ctenomys talarum (Rodentia, Octodontidae) in a natural grassland. Zeitschrift für Säugetierkunde 57:47-55.
13. COMPARATORE, V. M., N. O. MAGEIRA, AND C. BUSCH. 1991. Habitat relations in Ctenomys talarum (Caviomorpha, Octodontidae) in a natural grassland. Zeitschrift für Säugetierkunde 56:112-118.
14. COOK, E., T. BIRD, M. PETERSON, M. BARBETTI, B. BUCKLEY, R. D'ARRIGO, AND R. FRANCEY. 1992. Climatic change over the last millennium in Tasmania reconstructed from tree-rings. Holocene 2:205-217.
15. COOK, E., ET AL. 1991. Climate change in Tasmania inferred from a 1089-year tree-ring chronology of Huan Pine. Science 253:1266-1268.
16. COOPER, A., AND H. N. POINAR. 2000. Ancient DNA: do it right or not at all. Science 289:1139.
17. D'ELIA, G., E. P. LESSA, AND J. A. COOK 1996. Molecular phylogeny of tuco-tucos, genus Ctenomys (Rodentia: Octodontidae): evaluation of the mendocinus species group and the evolution of asymmetric sperm. Journal of Mammalian Evolution 6:19-38.
18. DODSON, P., AND D. WEXLAR. 1979. Taphonomic investigation of owl pellets. Paleobiology 5:275-284.
19. GALLARDO, M. H., AND N. KÖHLER. 1992. Genetic divergence in Ctenomys (Rodentia, Ctenomyidae) from the Andes of Chile. Journal of Mammalogy 73:99-105.
20. GALLARDO, M. H., AND N. KÖHLER. 1994. Demographic changes and genetic losses in populations of a subterranean rodent (Ctenomys maulinus brunneus) affected by a natural catastrophe. Zeitschrift für Säugetierkunde 59:358-365.
21. GALLARDO, M. H., N. KÖHLER, AND C. ARANEDA. 1995. Bottleneck effects in local populations of fossorial Ctenomys (Rodentia, Ctenomyidae) affected by vulcanism. Heredity 74:638-646.
22. GILPIN, M. E., AND M. E. SOULÉ. 1986. Minimum viable populations: processes of species extinction. Pp. 19-34 in Conservation biology: the science of scarcity and diversity (M. E. Soulé, ed.). Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts.
23. HADLY, E. A. 1996. Influence of late-Holocene climate on northern Rocky Mountain mammals. Quaternary Research 46:298-310.
24. HADLY, E. A. 1997. Evolutionary and ecological response of pocket gophers (Thomomys talpoides) to late-Holocene climatic change. Biological Journal of the Linnean Society 60:277-296.
25. HADLY, E. A. 1999. Fidelity of terrestrial vertebrate fossils to a modern ecosystem. Palaeogeography, Palaeoclimatology, Palaeoclimatology 149:395-415.
26. HADLY, E. A., M. H. KOHN, J. A. LEONARD, AND R. K. WAYNE. 1998. A genetic record of population isolation in pocket gophers during Holocene climatic change. Proceedings of the National Academy of Sciences 95:6893-6896.
27. HANDT, O., M. HÖSS, M. KRINGS, AND S. PÄÄBO. 1994. Ancient DNA: methodological challenges. Experentia 50:524-529.
28. HEUSSER, C. J. 1995. Three late Quaternary pollen diagrams from southern Patagonia and their palaecological implications. Palaeogeography, Palaeoclimatology, Palaeoclimatology 118:1-24.
29. HILTON-TAYLOR, C. (COMP.). 2000. 2000 IUCN red list of threatened species. World Conservation Union (IUCN), Gland, Switzerland.
30. HOELZEL, A. R., ET AL. 1993. Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. Journal of Heredity 84:443-449.
31. HOFFMANN, J. A. J. 1975. Atlas climatico de America del Sur. World Meterological Organization, United Nations Educational, Scientific, and Cultural Organization (UNESCO), Geneva, Switzerland.
32. HÖSS, M., AND S. PÄÄBO. 1993. DNA extraction from Pleistocene bones by a silica-based purification method. Nucleic Acid Research 21:3913-3914.
33. HUGHES, M. K., AND H. F. DIAZ. 1994. The Medieval Warm Period. Kluwer Academic Publishers, Dordrecht, The Netherlands.
34. JABLONSKI, D. 1991. Extinctions: a paleontological perspective. Science 253:754-757.
35. JOHNSGARD, P. A. 1990. Hawks, eagles, and falcons of North America. Smithsonian Institution Press, Washington, D.C.
36. KEIGWIN, L. 1996. The Little Ice Age and Medieval Warm Period in the Sargasso Sea. Science 274:1504-1508.
37. KELLER, L. F. 1998. Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240-250.
38. KITZBERGER, T., T. T. VEBLEN, AND R. VILLALBA. 1997. Climatic influences on fire regimes along a rain forest-to-xeric woodland gradient in northern Patagonia, Argentina. Journal of Biogeography 24:35-47.
39. LACEY, E. A. 2000. Spatial and social systems of sub-terranean rodents. Pp. 257-296 in Life underground: the biology of subterranean rodents (E. A. Lacey, J. L. Patton, and G. N. Cameron, eds.). University of Chicago Press, Chicago, Illinois.
40. LACEY, E. A. 2001. Microsatellite variation in solitary and social tuco-tucos: molecular properties and population dynamics. Heredity 86:628-637.
41. LACEY, E. A., S. H. BRAUDE, AND J. R. WIECZOREK. 1997. Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). Journal of Mammalogy 78:556-562.
42. LACEY, E. A., J. L. PATTON, AND G. N. CAMERON (EDS.). 2000. Life underground: the biology of subterranean rodents. University of Chicago Press, Chicago, Illinois.
43. LAMB, H. H. 1965. The early medieval warm epoch and its sequel. Palaeogeography, Palaeoclimatology, Palaeoclimatology 1:13-37.
44. LAMB, H. H. 1977. Climatic history and the future. Metheun and Company Ltd., London, United Kingdom.
45. LANDE, R. 1988. Genetics and demography in biological conservation. Science 241:1455-1460.
46. LEONARD, J. A., R. K. WAYNE, AND A. COOPER. 2000. Population genetics of Ice Age brown bears. Proceedings of the National Academy of Sciences 97:1651-1654.
47. LESSA, E. P., AND J. A. COOK. 1998. The molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation. Molecular Phylogenetics and Evolution 9:88-99.
48. MADOERY, C. L., AND V. ROIG. 1995. The burrowing behavior of Ctenomys mendocinus (Rodentia). Mammalia 59:9-17.
49. MANCINI, M. V. 1998. Vegetational changes during the Holocene in extra-Andean Patagonia, Santa Cruz Province, Argentina. Palaeogeography, Palaeoclimatology, Palaeoclimatology 138:207-219.
50. MARKGRAF, V. 1983. Late and postglacial vegetation and paleoclimatic changes in subantarctic, temperate, and arid environments in Argentina. Palynology 7:43-70.
51. MARKGRAF, V., AND L. ANDERSON. 1994. Fire history of Patagonia: climate versus human change. Revista Instituto do Geografico São Paulo 15:35-47.
52. MARKGRAF, V., J. BETANCOURT, AND K. A. RYLANDER. 1997. Late Holocene rodent middens from Rio Limay, Neuquen Province Argentina. Holocene 7:325-329.
53. MASSON, V., ET AL. 2000. Holocene climate variability in Antarctica based on 11 ice-core isotopic records. Quaternary Research 54:348-358.
54. MCKINNEY, M. L. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495-516.
55. MILLER, S. D., J. ROTTMANN, K. J. RAEDEKE, AND R. D. TABER. 1983. Endangered mammals of Chile: status and conservation. Biological Conservation 25:335-352.
56. MIROL, P. M., S. MASCHERETTI, AND J. B. SEARLE. 2000. Multiple nuclear pseudogenes of mitochondrial cytochrome b in Ctenomys (Caviomorpha, Rodentia) with either great similarity to or high divergence from the true mitochondrial sequence. Heredity 84:538-547.
57. NEVO, E. 1979. Adaptive convergence and divergence of subterranean mammals. Annual Review of Ecology and Systematics 10:269-308.
58. O'BRIEN, S. J. 1994. A role for molecular genetics in biological conservation. Proceedings of the National Academy of Sciences 91:5748-5755.
59. O'BRIEN, S. J., ET AL. 1985. Genetic basis for species vulnerability in the cheetah. Science 227:1428-1431.
60. OU, C.-Y., J. C. MOORE, AND G. SCHOCHETMAN. 1991. Use of UV irradiation to reduce false positivity in polymerase chain reaction. Biotechniques 10:442-446.
61. PÄÄBO, S. 1989. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. Proceedings of the National Academy of Sciences 86:1939-1943.
62. PASKOFF, R. P. 1977. Quaternary of Chile: the state of research. Quaternary Research 8:2-31.
63. PEARSON, O. P. 1959. Biology of the subterranean rodents, Ctenomys, in Peru. Memorias del Museo de Historia Natural 'Javier Prado' 9:1-56.
64. PEARSON, O. P. 1984. Taxonomy and natural history of some fossorial rodents of Patagonia, southern Argentina. Journal of Zoology (London) 202:225-237.
65. PEARSON, O. P. 1995. Annotated keys for identifying small mammals living in or near Nahuel Haupi National Park or Lanín National Park, southern Argentina. Mastozoologia Neotropical 2:99-148.
66. PEARSON, O. P., AND M. I. CHRISTIE. 1985. Los tuco-tucos (gennnero Ctenomys) de los Parques Nacionales Lanin y Nahuel Huapi, Argentina. Historia Natural 5:337-344.
67. PEARSON, O. P., AND A. K. PEARSON. 1993. La fauna de mamiferos pequeños de Cueva Traful I, Argentina: pasado y presente. Praehistoria 1:211-224.
68. PENDALL, E., V. MARKGRAF, J. W. C. WHITE, AND M. DREIER. 2001. Multiproxy record of late Pleistocene-Holocene climate and vegetation changes from a peat bog in Patagonia. Quaternary Research 55:168-178.
69. PORDER, S. J., A. PAYTAN, AND E. A. HADLY. 2003. Mapping the origin of faunal assemblages using strontium isotopes. Paleobiology.
70. REIG, O. A., C. BUSCH, M. O. ORTELLS, AND J. R. CONTRERAS. 1990. An overview of evolution, systematics, population biology, cytogenetics, molecular biology and speciation in Ctenomys. Fifth International Theriological Congress: evolution of subterranean mammals at the organismal and molecular levels, Rome, Italy 5:71-96.
71. SACCHERI, I., M. KUUSSAARI, M. KANKARE, P. VIKMAN, W. FORTELIUS, AND I. HANSKI. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491-494.
72. SAMBROOK, J., E. F. FRITCH, AND T. MANIATIS. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
73. SARKAR, G., AND S. S. SOMER. 1993. Removal of DNA contamination in polymerase chain reaction reagents by ultraviolet irradiation. Methods in Enzymology 218:381-388.
74. SLADE, R. W., C. MORITZ, A. R. HOELZEL, AND H. R. BURTON. 1998. Molecular population genetics of the southern elephant seal Mirounga leonina. Genetics 149:1945-1957.
75. STINE, S. 1994. Extreme and persistent drought in California and Patagonia during medieval time. Nature 369:546-549.
76. SWOFFORD, D. L. 2002 PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts.
77. VASSALLO, A. I. 1998. Functional morphology, comparative behaviour, and adaptation in two sympatric subterranean rodents genus Ctenomys (Caviomorpha: Octodontidae). Journal of Zoology (London) 244:415-427.
78. VEBLEN, T. T., C. DONOSO, T. KITZBERGER, AND A. J. REBERTUS. 1996. Ecology of southern Chilean and Argentinean Nothofagus forests. Pp. 293-353 in The ecology and biogeography of Nothofagus forests (T. T. Veblen, R. S. Hill, and J. Read, eds.). Yale University Press, New Haven, Connecticut.
79. VEBLEN, T. T., R. S. HILL, AND J. READ. 1996. Epilogue: commonalities and needs for future research. Pp. 387-397 in The ecology and biogeography of Nothofagus forests (T. T. Veblen, R. S. Hill, and J. Read, eds.). Yale University Press, New Haven, Connecticut.
80. VEBLEN, T. T., AND D. C. LORENZ. 1988. Recent vegetation changes along the forest/steppe ecotone of northern Patagonia. Annals of the Association of American Geographers 78:93-111.
81. VEBLEN, T. T., M. MERMOZ, C. MARTIN, AND E. RAMILO. 1989. Effects of exotic deer on forest regeneration and composition in northern Patagonia. Journal of Applied Ecology 26:711-724.
82. VILLALBA, R. 1990. Climatic fluctuations in northern Patagonia during the last 1000 years as inferred from tree-ring records. Quaternary Research 34:346-360.
83. VILLALBA, R. 1994. Tree-ring and glacial evidence for the medieval warm epoch and the Little Ice Age in southern South America. Climate Change 26:183-197.
84. VILLALBA, R., R. L. HOLMES, AND J. A. BONINSEGNA. 1992. Spatial patterns of climate and tree growth variations in subtropical northwestern Argentina. Journal of Biogeography 19:631-649.
85. WAN, C.-Y., AND T. A. WILKINS. 1993. Spermidine facilitates PCR amplification of target DNA. PCR Methods and Applications 2:208-210.
86. WAYNE, R. K., J. A. LEONARD, AND A. COOPER. 1999. Full of sound and fury: the recent history of ancient DNA. Annual Review of Ecology and Systematics 30:457-477.
87. WEBB, R. H., AND J. L. BETANCOURT. 1990. The spatial and temporal distribution of radiocarbon ages from packrat middens. Pp. 85-102 in Packrat middens: the last 40,000 years of biotic change (J. J. Betancourt, T. R. van Devender, and P. S. Martin, eds.). University of Arizona Press, Tucson.
88. YANG, D. Y., B. ENG, J. S. WAYE, H. C. DUDAR, AND S. R. SAUNDERS. 1998. Technical note: improved DNA extraction from ancient bones using silicabased spin columns. American Journal of Physical Anthropology 105:539-543.