Ancient DNA evidence of Iberian lynx palaeoendemism

Quaternary Science Reviews

Volumn 112, Issue , 2015, Pages 172-180

  Rodríguez Varela, Ricardo ^a,b   Tagliacozzo, Antonio ^c   Ureña, Irene ^a   García, Nuria ^a,b   Crégut Bonnoure, Evelyne ^d,g   Mannino, Marcello A ^e   Arsuaga, Juan Luis ^a,b   Valdiosera, Cristina ^a,f  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c Soprintendenza al Museo Nazionale Preistorico ed Etnografico LPigorini   (Italy)

^d Muséum Requien   (France)

^e MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^f LA TROBE UNIVERSITY   (Australia)

^g CNRS   (France)

Author keywords

Ancient DNA; Eurasian lynx; Iberian lynx; Mitochondrial DNA; Palaeoendemism

Indexed keywords

GEOGRAPHICAL DISTRIBUTION;

ANCIENT DNAS; EURASIAN LYNX; IBERIAN LYNX; MITOCHONDRIAL DNA; PALAEOENDEMISM;

DNA;

CARNIVORE; DNA; ENDANGERED SPECIES; ENDEMISM; FELID; FOSSIL RECORD; GENE EXPRESSION; GEOGRAPHICAL DISTRIBUTION; HOLOCENE; MORPHOLOGY;

IBERIAN PENINSULA; SPAIN;

FELIDAE; LYNX; LYNX LYNX;

EID: 84922991618     PISSN: 02773791     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.quascirev.2015.01.009     Document Type: Article

References (88)

1. Alda F., Inogés J., Alcaraz L., Oria J., Aranda A., Doadrio I. Looking for the Iberian lynx in central Spain: a needle in a haystack?. Anim. Conserv. 2008, 1:297-305.
2. Allentoft M.E., Oskam C., Houston J., Hale M.L., Gilbert M.T.P., Rasmussen M., Spencer P., Jacomb C., Willerslev E., Holdaway R.N., Bunce M. Profiling the dead: generating microsatellite data from fossil bones of extinct megafauna - protocols, problems, and prospects. PLoS One 2011, 6:e16670.
3. Aquadro C.F., Greenberg B.D. Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics 1983, 103:287-312.
4. Avise J.C., Walker D. Species realities and numbers in sexual vertebrates: perspectives from an asexually transmitted genome. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:992-995.
5. Baldeón A. El Abrigo de Axlor (Bizkaia, País Vasco). Munibe 1999, 51:9-121.
6. Beltrán J.F., Rice J.E., Honeycutt R.L. Taxonomy of the Iberian lynx. Nature 1996, 379:407-408.
7. Blasco M.-F. In the pursuit of game: the Mousterian cave site of Gabasa I in the Spanish Pyrenees. J.Anthr. Res. 1997, 53:177-217.
8. Bonifay M.-F. Carnivores quaternaires du Sud-Est de la France. Mem. Mus. Nat. Hist. Nat., Nouv. Ser., A 1971, XXI. fasc. 2.
9. Bonifay M.-F. Le gisement de la Baume de Valorgues à Saint-Quentin-la-Poterie (Gard). (Paléolithique supérieur final et Epipaléolithique) II. La grande faune. Gall. Préhist. 1978, 21(1):123-142.
10. Boule M. Les grottes de Grimaldi 1906, vol. 1(4):237-362. Imprimerie de Monaco.
11. Boule M. Géologie et paléontologie (suite). Les grottes de Grimaldi (Baousé-Roussé) 1910, vol. 1:157-236. Monaco.
12. Boule M., Villeneuve L.de La Grotte de L'Observatoire à Monaco 1927, vol. 1:113. Archives de l'Institut de Paléontologie Humaine, Paris.
13. Bronk Ramsey C. Bayesian analysis of radiocarbon dates. Radiocarbon 2009, 51(1):337-360.
14. Brown J.R., Beckenbach A.T., Smith M.J. Intraspecific DNA sequence variation of the mitochondrial control region of white sturgeon (Acipenser transmontanus). Mol. Biol. Evol. 1993, 10:326-341.
15. Callou C. Modification de l'aire de répartition du lapin (Oryctolagus cuniculus) en France et en Espagne, du Pléistocène à l'époque actuelle: État de la question. Anthropozoologica 1995, 21:95-114.
16. Callou C. De la garenne au clapier: étude archéozoologique du Lapin en Europe occidentale. Mem. Mus. Nat. Hist. Nat. (Fr.) 2002, 189:1-358.
17. Cardini L. Gli strati mesolitici e paleolitici della Caverna della Arene Candide. Riv. Studi. Liguria 1947, anmo XII(1-3):3-11. (1946).
18. Casas-Marce M., Soriano L., López-Bao J.V., Godoy J.A. Genetics at the verge of extinction: insights from the Iberian lynx. Mol. Ecol. 2013, 22:5503-5515.
19. Cassoli P.F., Tagliacozzo A. Imacromammiferi dei livelli tardopleistoceni delle Arene Candide (Savona, Italia): considerazioni paleontologiche e archeozoologiche. Quat. Nova 1994, 4:101-262.
20. Cooper A., Rhymer J.D., James H.F., Olson S.L., McIntosh C.E., Sorenson M.D., Fleischer R.C. Ancient DNA and island endemics. Nature 1996, 381:484.
21. Dabey J., Knapp M., Glocke I., Gansauge M.T., Weihmann A., Nickel B., Valdiosera C., Garcia N., Pääbo S., Arsuaga J.L., Meyer M. Acomplete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultra-short DNA fragments. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(39):15758-15763.
22. Dalén L., Nyström V., Valdiosera C., Germonpre M., Sablin M., Turner E., Angerbjörn A., Arsuaga J.L., Götherström A. Ancient DNA reveals lack of postglacial habitat tracking in the arctic fox. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6726-6729.
23. Deffontaine V., Libois R., Kotlík P., Sommer R., Nieberding C., Paradis E., Searle J.B., Michaux J.R. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol. Ecol. 2005, 14:1727-1739.
24. Delibes M. Feeding ecology of the Spanish lynx in the Coto Doñana (Huelva, Spain). Acta. Theriol. 1980, 25:309-324.
25. Den Tex R.-J., Maldonado J.E., Thorington R., Leonard J.A. Nuclear copies of mitochondrial genes: another problem for ancient DNA. Genetica 2010, 138:979-984.
26. Excoffier L., Laval G., Schneider S. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 2005, 1:47-50.
27. Fernandes C., Ginja C., Pereira I., Tenreiro R., Bruford M., Santos-Reis M. Species-specific mitochondrial DNA markers for identification of non-invasive samples from sympatric carnivores in the Iberian Peninsula. Conserv. Genet. 2008, 9:681-690.
28. Ferrer M., Negro J.J. The near extinction of two large European predators: super specialists pay a price. Conserv. Biol. 2004, 18:344-349.
29. Fiore I., Pino-Uria B., Tagliacozzo A. L'exploitation des petits animaux au Paléolithique supérieur-Mésolithique en Italie: l'exemple de la Grotta del Santuario della Madonna de Praia a Mare (Cosenza, Italie). Petits animaux et sociétés humaines. Du complément alimentaire aux ressources utilitaire, XXIV Rencontres Internationales d'archéologie et d'histoire d'Antibes, Antibes 23-25 octobre 2003 2004, 417-430. APDCA, Antibes. J.P. Brugal, J. Desse (Eds.).
30. Fordham D.A., Akçakaya H.R., Brook B.W., Rodríguez A., Alves P.C., Civantos E., Triviño M., Watts M.J., Araújo M.B. Adapted conservation measures are required to save the Iberian lynx in a changing climate. Nat. Clim. Change 2013, 3:899-903.
31. Frankham R., Ballou J.D., Briscoe D.A. Introduction to Conservation Genetics 2002, Cambridge University Press, Cambridge, UK.
32. Gay S.W., Best T.L. Relationships between abiotic variables and geographic variation in skulls of pumas (Puma concolor: Mammalia, Felidae) in North and South America. Zool. J. Linn. Soc. 1996, 117(3):259-282.
33. Gil-Sánchez J.M., Ballesteros-Duperon E., Bueno-Segura J.F. Feeding ecology of the Iberian lynx Lynx pardinus in eastern Sierra Morena (southern Spain). Acta. Theriol. 2006, 51:85-90.
34. Gil-Sanchez J.M., McCain E.B. Former range and decline of the Iberian lynx (Lynx pardinus) reconstructed using verified records. J.Mammal. 2011, 92:1081-1090.
35. Goldstein P.Z., DeSalle R. Calibrating phylogenetic species formation in a threatened insect using DNA from historical specimens. Mol. Ecol. 2003, 12:1993-1995.
36. Grayson D.K., Delpech F. The evidence for Middle Palaeolithic scavenging from Couche VIII, Grotte Vaufrey (Dordogne, France). J.Archaeol. Sci. 1994, 21:359-375.
37. Grayson D.K., Delpech F. Changing diet breadth in the early Upper Paleolithic of southwestern France. J.Archaeol. Sci. 1998, 25:1119-1129.
38. Griffith B., Scott J.M., Carpenter J.W., Reed C. Translocation as a species conservation tool: status and strategy. Science 1989, 245:477-480.
39. Guilaine J., Rencoule G., Vaquer J., Passelac M., Vigne J.D. Carsac une agglomération protohistorique en Languedoc 1986, Centre d'Anthropologie des Sociétés Rurales, Toulouse.
40. Hellborg L., Walker C.W., Rueness E.K., Stacy J.E., Kojola I., Valdmann H., Vila C., Zimmerman B., Jakobsen K.S., Ellegren H. Differentiation and levels of genetic variation in northern European lynx (Lynx lynx) populations revealed by microsatellites and mitochondrial DNA analysis. Conserv. Genet. 2002, 3:97-111.
41. Hoelzel A.R., Dover G.A. Evolution of the cetacean mitochondrial D-loop region. Mol. Biol. Evol. 1991, 8:475-493.
42. Hoelzel A.R., Lopez J.V., Dover G.A., O'Brien S.J. Rapid evolution of a heteroplasmic repetitive sequence in the mitochondrial DNA control region of carnivores. J.Mol. Evol. 1994, 39:191-199.
43. Hofreiter M. Long DNA sequences and large data sets: investigating the Quaternary via ancient DNA. Quat. Sci. Rev. 2008, 27:2586-2592.
44. Iriarte J.A., Redford K.H., Franklin W.L., Johnson W.E. Biogeographic variation of food habits and body size of the American puma (Felis concolor). Oecologia 1990, 82:185-190.
45. IUCN IUCN Red List of Threatened Species. Version 2012.1 2012, Downloaded on 05 October 2012. http://www.iucnredlist.org.
46. Johns G.C., Avise J.C. Acomparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol. Biol. Evol. 1998, 15:1481-1490.
47. Johnson W.E., Eizirik E., Pecon-Slattery J., Murphy W.J., Antunes A., Teeling E., O'Brien S.J. The Late Miocene radiation of modern Felidae: a genetic assessment. Science 2006, 311:73-77.
48. Johnson W.E., Godoy J.A., Palomares F., Delibes M., Fernandes M., Revilla E., O'Brien S.J. Phylogenetic and phylogeographic analysis of Iberian lynx populations. J.Hered. 2004, 95:19-28.
49. Kurtén B., Granqvist E. Fossil pardel lynx (Lynx pardina spelaea Boule) from a cave in southern France. Ann. Zool. Fenn. 1987, 24:39-43.
50. Leonard J.A. Ancient DNA applications for wildlife conservation. Mol. Ecol. 2008, 17:4186-4196.
51. Lopez J.V., Culver M., Stephens J.C., Johnson W.E., O'Brien S.J. Rates of nuclear and cytoplasmic mitochondrial DNA sequence divergence in mammals. Mol. Biol. Evol. 1997, 14:277-286.
52. López-Martínez N. The lagomorph fossil record and the origin of the European rabbit. Lagomorph Biology: Evolution, Ecology, and Conservation 2008, 26-47. Springer, Amsterdam, The Netherlands. P.C. Alves, N. Ferrand, K. Hackländer (Eds.).
53. Masuda R., Yoshida M.C., Shinyashiki F., Bando G. Molecular phylogenetic status of the iriomote cat Felis iriomotensis, inferred from mitochondrial DNA sequence analysis. Zool. Sci. 1994, 11:597-604.
54. Nowell K., Jackson P. Wild Cats: Status Survey and Conservation Action Plan 1996, IUCN Publications. Burlington Press, Cambridge.
55. Palomares F. Vegetation structure and prey abundance requirements of the Iberian lynx: implications for the design of reserves and corridors. J.Appl. Ecol. 2001, 38:9-18.
56. Palomares F., Delibes M., Ferreras P., Fedriani J.M., Calzada J., Revilla E. Iberian lynx in a fragmented landscape: pre-dispersal, dispersal and post-dispersal habitats. Conserv. Biol. 2000, 14:809-818.
57. Palomares F., Delibes M., Revilla E., Calzada J., Fedriani J.M. Spatial ecology of Iberian lynx and abundance of European rabbits in southwestern Spain. Wildl. Monogr. 2001, 148:1-36.
58. Quam R.M., Arsuaga J.L., Bermúdez de Castro J.M., Díez J.C., Lorenzo C., Carretero J.M., García N., Ortega A. Human remains from Valdegoba Cave (Huermeces, Burgos, Spain). J.Hum. Evol. 2001, 41:385-435.
59. Reimer P.J., Bard E., Bayliss A., Beck J.W., Blackwell P.G., Ramsey B.C., Buck C.E., Cheng H., Edwards R.L., Friedrich M., Grootes P.M., Guilderson T.P., Haflidason H., Hajdas I., Hatté C., Heaton T.J., Hoffman D.L., Hogg A.G., Hughen K.A., Kaiser K.F., Kromer B., Manning S.W., Niu M., Reimer R.W., Richards D.A., Scott E.M., Southon J.R., Staff R.A., Turney C.S.M., van der Plicht J. IntCal13 and Marine13 radiocarbon age calibration curves 0-50,000 years cal BP. Radiocarbon 2013, 55(4):1869-1887.
60. Rodríguez A., Delibes M. Current range and status of the Iberian lynx Felis pardina Temminck, 1824 in Spain. Biol. Conserv. 1992, 61:189-196.
61. Rodríguez A., Delibes M. Internal structure and patterns of contraction in the geographic range of the Iberian lynx. Ecography 2002, 25:314-328.
62. Rodríguez R., Ramírez O., Valdiosera C.E., García N., Alda F., Madurell-Malapeira J., Marmi J., Doadrio I., Willerslev E., Götherström A., Arsuaga J.L., Thomas M.G., Lalueza-Fox C., Dalén L. 50,000 years of genetic uniformity in the critically endangered Iberian lynx. Mol. Ecol. 2011, 20:3785-3795.
63. Rosado-Méndez N.Y., Lloveras L., Daura J., Nadal J., Sanz M. Predator agents and Leporid accumulations: the case of Terrasses de la Riera dels Canyars (Gavà, Barcelona, Spain). J.Archaeol. Method. Theory 2014, 1-26.
64. Rueness E.K., Naidenko S., Trosvik P., Stenseth N.C. Large-scale genetic structuring of a widely distributed carnivore - the Eurasian Lynx (Lynx lynx). PLoS One 2014, 9(4):e93675. 10.1371/journal.pone.0093675.
65. Schmitt T., Varga Z. Extra-Mediterranean refugia: the rule and not the exception?. Front. Zool. 2012, 9:22.
66. Schwartz M.K., Pilgrim K.L., McKelvey K.S., Lindquist E.L., Claar J.J., Loch S., Ruggiero L.R. Hybridization between Canada lynx and bobcats: genetic results and management implications Canada lynx. Conserv. Genet. 2004, 6:349-355.
67. Shepherd L.D., Lambert D.M. Ancient DNA and conservation: lessons from the endangered kiwi of New Zealand. Mol. Ecol. 2008, 17:2174-2184.
68. Sindičić M., Gomerčić T., Galov A., Polanc P., Huber D., Slavica A. Repetitive sequences in Eurasian lynx (Lynx lynx L.) mitochondrial DNA control region. Mitochondrial DNA 2012, 23(3):201-207.
69. Smulders M.J.M., Snoek L.B., Booy G., Vosman B. Complete loss of MHC genetic diversity in the common hamster (Cricetus cricetus) population in The Netherlands. Consequences for conservation strategies. Conserv. Genet. 2003, 4:441-451.
70. Sommer R.S., Benecke N. Late Pleistocene and Holocene development of the felid fauna (Felidae) of Europe: a review. J.Zool. 2006, 269:7-19.
71. Sommer R.S., Nadachowski A. Glacial refugia of mammals in Europe: evidence from fossil records. Mamm. Rev. 2006, 36:251-265.
72. Tagliacozzo A., Cassoli P.F. La macrofaune del l'Abri Soman (Val d'Adige - Italie). Preist. Alp. 1993, 28:181-192.
73. Tagliacozzo A., Zeppieri F., Fiore I., Spinapolice E., Lucchese A.D. Archaeozoological evidence of subsistence strategies during the Gravettian at Riparo Mochi (Balzi Rossi, Ventimiglia, Imperia - Italy). Quat. Int. 2011, 252:142-154.
74. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
75. Thomas C.D. Translocation of species, climate change, and the end of trying to recreate past ecological communities. Trends. Ecol. Evol. 2011, 26:216-221.
76. Valdiosera C.E., García N., Anderung C., Dalén L., Crégut-Bonnoure E., Kahlke R.D., Stiller M., Brandström M., Thomas M.G., Arsuaga J.L., Götherström A., Barnes I. Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Mol. Ecol. 2007, 16:5140-5148.
77. Valensi P. Les grands mammifères de la grotte du Lazaret, Nice. Etude paléontologique et biostratigraphique des Carnivores. Archéozoologie des grandes faunes 1994, (PhD thesis), National Museum of Natural History, Paris.
78. Valensi P., Psathi E. Faunal exploitation during the Middle Palaeolithic in South-eastern France and North-western Italy. Int. J. Osteoarchaeol. 2004, 14:256-272.
79. Van den Brink F.-H. Distribution and speciation of some carnivores - 2. Mamm. Rev. 1973, 3:85-95.
80. Van den Brink F.-H. Distribution and speciation of some carnivores. Mamm. Rev. 1970, 1:67-78.
81. Van den Brink F.-H. Le lynx pardelle en France. Bull. Soc. Sci. Nat. Nîmes 1971, 51:109-117.
82. Vargas A., Sanchez I., Martinez F., Rivas A., Godoy J.A., Roldan E., Simon M.A., Serra R., Perez M.J., Ensenat C., Delibes M., Aymerich M., Sliwa A., Breitenmoser U. The Iberian lynx Lynx pardinus conservation breeding program. Int. Zoo. Yearb. 2008, 42:190-198.
83. Vigne J.D. La faune des vertébrés. Le Laouret et la Montagne d'Alaric à la fin de l'âge du Bronze. Un hameau abandonné entre Floure et Monze (Aude) 1996, 197-239. Centre d' Anthropologie, Toulouse. J. Gasco (Ed.).
84. Vigne J.D., Pascal M. Le Lynx pardelle Lynx pardinus (Temnick, 1827). Evolution de la faune de Vertébrès en France métropolitaine depuis le début de Holocène. Invasions et extinctions 2003, 87-89. Institut National de la Recherche Agronomique, Centre National de la Recherche scientifique, Muséum National d'Histoire Naturelle de Paris. M. Pascal, O. Lorvelec, J.D. Vigne, P. Keith, P. Clergeau (Eds.).
85. Werdelin L. The evolution of lynxes. Ann. Zool. Fenn. 1981, 18:37-71.
86. Wiggington J.D., Dobson F.S. Environmental influences on geographic variation in body size of western bobcats. Can. J. Zool. 1999, 77:802-813.
87. Yang D., Eng B., Waye J., Dudar J., Saunders S. Technical note: improved DNA extraction from ancient bones using silica based spin columns. Am. J. Phys. Anthropol. 1998, 105:539-554.
88. Yom-Tov Y., Yom-Tov S., MacDonald D., Yom-Tov E. Population cycles and changes in body size of the lynx in Alaska. Oecologia 2007, 152:239-244.