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Phylogeny, diet, and habitat of an extinct ground sloth from Cuchillo Curá, Neuquén Province, southwest Argentina

Published online by Cambridge University Press:  20 January 2017

Michael Hofreiter
Affiliation:
Max Planck Institute for Evolutionary Anthropology, Inselstrasse 22, D-04103 Leipzig, Germany
Julio L. Betancourt*
Affiliation:
U.S. Geological Survey, Desert Laboratory, 1675 W. Anklam Rd., Tucson, AZ 85745, USA
Alicia Pelliza Sbriller
Affiliation:
Laboratorio de Microhistologia, INTA-EEA Bariloche, CC 277 (R8400AMC) Bariloche, Argentina
Vera Markgraf
Affiliation:
Vera Markgraf, INSTAAR, University of Colorado, Boulder, CO 80309-0450, USA
H. Gregory McDonald
Affiliation:
Geologic Resources Division, National Park Service, 7333 West Jefferson Avenue, P.O. Box 25287, Denver, CO 80225, USA
*
*Corresponding author. Fax: +1-520-670-6806. Email Address:jlbetanc@usgs.gov

Abstract

Advancements in ancient DNA analyses now permit comparative molecular and morphological studies of extinct animal dung commonly preserved in caves of semiarid regions. These new techniques are showcased using a unique dung deposit preserved in a late glacial vizcacha (Lagidium sp.) midden from a limestone cave in southwestern Argentina (38.5° S). Phylogenetic analyses of the mitochondrial DNA show that the dung originated from a small ground sloth species not yet represented by skeletal material in the region, and not closely related to any of the four previously sequenced extinct and extant sloth species. Analyses of pollen and plant cuticles, as well as analyses of the chloroplast DNA, show that the Cuchillo Curá ground sloth browsed on many of the same herb, grass, and shrub genera common at the site today, and that its habitat was treeless Patagonian scrub-steppe. We envision a day when molecular analyses are used routinely to supplement morphological identifications and possibly to provide a time-lapse view of molecular diversification.

Type
Articles
Copyright
Elsevier Science (USA)

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References

Altschul, S.F, Madden, T.L, Schäffer, A.A, Zhang, J, Zhang, Z, Miller, W, and Lipman, D.J Gapped BLAST and PSI BLAST. a new generation of protein database search programs. Nucleic Acids Research 25, (1997). 3389 3402.Google Scholar
Anghilante, C.D Resultados bioespeológicos preliminares sobre el sistema de Cuchillo Curá. Salamanca 3, (1987). 13 18. (http://www.petersen.com.ar/gea/salam.htm)Google Scholar
Betancourt, J.L, and Saavedra, B Nuevo método paleoecológico para el estudio de zonas áridas en Sudamérica. paleomadrigueras de roedores (New paleoecological method for Quaternary studies in arid lands of South America: rodent middens). Revista Chilena de Historia Natural 75, (2002). 527 546.Google Scholar
Betancourt, J.L, Latorre, C, Rech, J.A, Quade, J, and Rylander, K.A A 22,000-yr record of monsoonal precipitation from northern Chile’s Atacama Desert. Science 289, (2000). 1542 1546.CrossRefGoogle Scholar
Borrero, L La extinción de la megafauna en la Patagonia. Anales del Instituto de la Patagonia. Serie Ciencias Humanas 25, (1997). 89 102.Google Scholar
Burmeister, H Nothropus priscus, ein bisher unbekanntes fossilies Faultier. Sitzungsberichte der Koniglich Preussischen Akademie der Wissenschaften zu Berlin 28, (1882). 613 620.Google Scholar
Burmeister, H Berichtigung zu Coelodon. Sitzungsberichte der Koniglich Preussischen Akademie der Wissenschaften zu Berlin 2, (1885). 567 573.Google Scholar
Burmeister, H Weitere bemerkungen uber Coelodon. Sitzungsberichte der Koniglich Preussischen Akademie der Wissenschaften zu Berlin 18, (1886). 357 358.Google Scholar
Burmeister, H Nochmalige berichtigung zu Coelodon. Sitzungsberichte Konig. Preussischen Akademie der Wissenschafter Zu Berlin 50, (1886). 1127 1132.Google Scholar
Burmeister, H Neue beobachtungen an Coelodon. Sitzungsberichte Konig. Preussischen Akademie der Wissenschafter Zu Berlin 42, (1887). 857 862.Google Scholar
Cartelle, C, and Bohorquez, G.A Desricao das pre-maxilas de Nothrotherium maquinense (Lund) Lydekker, 1889 (Edentada, megalonychidae) e de Eremotherium laurillardi (Lund) Cartelle and Bohorquez, 1982. Edentata, Megatheridae). Iheringia 11, (1986). 9 14.Google Scholar
Cooper, A, Mourer-Chauvire, C, Chambers, G.K, von Haeseler, A, Wilson, A.C, and Pääbo, S Independent origins of New Zealand moas and kiwi. Proceedings of the National Academy of Science 89, (1992). 8741 8744.CrossRefGoogle Scholar
Cooper, A, Lalueza-Fox, C, Anderson, S, Rambaut, A, Austin, J, and Ward, R Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution. Nature 409, (2001). 704 707.Google Scholar
D’Antoni, H.L Pollen analysis of Gruta del Indio. Quaternary of South America and Antarctic Peninsula 1, (1983). 83 104.Google Scholar
Davis, O.K., Agenbroad, L.D., Martin, P.S., and Mead, J.I., (1984). The Pleistocene dung blanket of Bechan Cave, Utah. Carnegie Museum of Natural History Special Publication 267–282.Google Scholar
Elzerad, L Geologia del sistema de cavernas del Cordon Cuchillo Curá. Salamanca 3, (1987). 3 11.Google Scholar
Frailey, C.D Late Miocene and Holocene mammals, exclusive of the Notoungulata, of the Rio Acre Region, western Amazonia. Natural History Museum of Los Angeles County, Contributions in Science 374, (1986). 1 46.Google Scholar
Garcia, A, and Lagiglia, H A 30,000 year old megafauna dung layer from Gruta del Indio (Mendoza, Argentina). Current Research in the Pleistocene 16, (1999). 116 118.Google Scholar
Greenwood, A.D, and Pääbo, S Nuclear insertion sequences of mitochondrial DNA predominate in hair but not in blood of elephants. Molecular Ecology 8, (1999). 133 137.CrossRefGoogle Scholar
Greenwood, A, Castresana, J, Feldmaier-Fuchs, G, and Pääbo, S A molecular phylogeny of two extinct sloths. Molecular Phylogenetics and Evolution 18, (2001). 94 103.CrossRefGoogle ScholarPubMed
Grosso, J La fauna intersticial de las cavernas de Cuchillo Curá, Neuquén, Republica Argentina. Salamanca 8, (1995). 5 11.Google Scholar
Handt, O, Richards, M, Trommsdorf, M, Kilger, C, Simanainen, J, Georgiev, O et al. Molecular genetic analysis of the Tyrolean ice man. Science 264, (1994). 1775 1778.CrossRefGoogle ScholarPubMed
Hansen, R.M Shasta ground sloth food habits, Rampart Cave, Arizona. Paleobiology 4, (1978). 302 319.Google Scholar
Harrington, M.R., (1933). Gypsum Cave, Nevada. Southwest Museum Papers No. 8, Los Angeles.Google Scholar
Heusser, C.J., (1971). Pollen and Spores of Chile. Univ. of Arizona Press, Google Scholar
Hofreiter, M, Poinar, H.N, Spaulding, W.G, Bauer, K, Martin, P.S, Possnert, G, and Pääbo, S A molecular analysis of ground sloth diet through the last glaciation. Molecular Ecology 9, (2000). 1975 1984.Google Scholar
Hofreiter, M, Jaenicke, V, Serre, D, von Haeseler, A, and Pääbo, S DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Research 29, (2001). 4793 4799.Google Scholar
Hofreiter, M, Serre, D, Poinar, H.N, Kuch, M, and Pääbo, S Ancient DNA. Nature Reviews in Genetics 2, (2001). 353 359.Google Scholar
Holmgren, C, Betancourt, J.L, Rylander, K.A, Roque, J, Tovar, O, Zeballos, H, Linares, E, and Quade, J Holocene vegetation history from fossil rodent middens near Arequipa, Peru. Quaternary Research 56, (2001). 242 251.CrossRefGoogle Scholar
Höss, M, and Pääbo, S DNA extraction from Pleistocene bones by a silica-based purification method. Nucleic Acids Research 21, (1993). 3913 3914.Google Scholar
Höss, M, Dilling, A, Currant, A, and Pääbo, S Molecular phylogeny of the extinct ground sloth Mylodon darwinii . Proceedings of the National Academy of Science 93, (1996). 181 185.Google Scholar
Kimura, M A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, (1980). 111 120.Google Scholar
Kuch, M, Rohland, N, Betancourt, J.L, Latorre, C, Steppan, S, and Poinar, H.N Molecular analysis of an 11,700-year old rodent midden from the Atacama Desert, Chile. Molecular Ecology 11, (2002). 913 924.Google Scholar
Kumar, S, Tamura, K, and Nei, M MEGA: Molecular Evolutionary Genetics Analysis, version 1.0 (user manual). (1993). The Pennsylvania State Univ, University Park, PA.Google Scholar
Laudermilk, J.D, and Munz, P.A Plants in the dung of Nothrotherium from Rampart and Muav caves, Arizona. Carnegie Institution of Washington Publication 487, (1934). 271 281.Google Scholar
Latorre, C.L, Betancourt, J.L, Rylander, K.A, and Quade, J.A Vegetation invasions into Absolute Desert. a 45,000-year rodent midden record from the Calama-Salar de Atacama Basins, Chile. Geological Society of America Bulletin 114, (2002). 349 366.2.0.CO;2>CrossRefGoogle Scholar
Latour, M.C., Pelliza Sbriller, A., (1981). Clave para la determinacion de la dieta de herbivoros en el noroeste de Patagonia. Revista de Investigaciones Agropecuarias INTA 16 Google Scholar
Long, A, Martin, P.S, and Lagiglia, H Ground sloth extinction and human occupation. Gruta del Indio. Radiocarbon 40, (1998). 693 700.CrossRefGoogle Scholar
Markgraf, V Late Pleistocene faunal extinctions in southern Patagonia. Science 228, (1985). 1110 1112.Google Scholar
Markgraf, V., D’Antoni, H., (1978). Pollen Flora of Argentina: Modern Pollen and Spore Types of Pteridophyta, Gymnospermae, and Angiospermae. Univ. of Arizona Press, Google Scholar
Markgraf, V, Betancourt, J.L, and Rylander, K.A Late-Holocene rodent middens from Rio Limay, Neuquén Province, Argentina. The Holocene 7, (1997). 325 329.CrossRefGoogle Scholar
Martin, P.S, Sabels, B.E, Shutler, R Jr. Rampart Cave coprolite and ecology of the Shasta ground sloth. American Journal of Science 259, (1961). 102 127.Google Scholar
McDonald, H.G., Muizon, C. de. (2002). The cranial anatomy of Thalassocnus (Xenarthra, Mammalia): a derived nothrothere from the Neogene of the Pisco Formation (Peru). Journal of Vertebrate Paleontology 22: 349365.Google Scholar
McKenna, M.C, and Bell, S.K Classification of mammals above the species level. (1998). Columbia Univ. Press, New York.Google Scholar
Mead, J.I The last 30,000 years of faunal history within the Grad Canyon, Arizona. Quaternary Research 15, (1981). 311 326.Google Scholar
Mead, J.I, Agenbroad, L.D, Phillips, A.M III, and Middleton, L.T Extinct mountain goat (Oreamnos harringtoni) in southeastern Utah. Quaternary Research 27, (1987). 323 331.CrossRefGoogle Scholar
Mead, J.I, Agenbroad, L.D, Davis, O.K, and Martin, P.S Dung of Mammuthus in the arid southwest, North America. Quaternary Research 25, (1986). 121 127.CrossRefGoogle Scholar
Merlin, V.E, and Rodriguez, N Estudios de hongos microscopios ambientales en una caverna del sistema de Cuchillo Cura, Neuquén. Salamanca 4, (1988). 43 48.Google Scholar
Meyer, S, Weiss, G, and von Haeseler, A Pattern of nucleotide substitution and rate heterogeneity in the hypervariable regions I and II of human mtDNA. Genetics 152, (1999). 1103 1110.Google Scholar
Moore, D.M Post-glacial vegetation in the South American territory of the giant ground sloth, Mylodon . Botanical Journal Linnean Society 77, (1978). 177 202.Google Scholar
Mourier, T, Hansen, A.J, Willerslev, E, and Arctander, P The Human Genome Project reveals a continuous transfer of large mitochondrial fragments to the nucleus. Molecular Biology and Evolution 18, 9 (2001). 1833 1837.Google Scholar
Movia, C.P., Ower, G.W., and Perez, C.E., (1992). Estudio de la Vegetacion Natural, Tomos I y II. Provincia del Neuquén, Ministerio de Economia y Hacienda, Subsecretaria de Recursons Naturales, Google Scholar
Nei, M, and Kumar, S Molecular Evolution and Phylogenetics. (2000). Oxford Univ. Press, New York.CrossRefGoogle Scholar
Patterson, B, Segall, W, Turnbull, W.D, and Gaudin, T.J The ear region in Xenarthrans (=Edentata: Mammalia) Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geology New Series 24, (1992). 1 79.Google Scholar
Pearson, O.P, and Christie, M.I Rodent guano (amberat) from caves in Argentina. Studies on Neotropical Fauna and Environment 28, (1993). 105 111.Google Scholar
Poinar, H.N, Hofreiter, M, Spaulding, G.W, Martin, P.S, Stankiewicz, B.A, Bland, H, Evershed, R.P, Possnert, G, and Paabo, S Molecular coproscopy. dung and diet of the extinct ground sloth Nothrotheriops shastensis . Science 281, (1998). 402 406.Google Scholar
Quaglia, P, Filipponi, A, Gatica, D, Orosco, W, and Salvo, A Los trabajos bioespeleológicos en las cavernas del sistema Cuchillo Curá. Salamanca 10, (1999). 30 32.Google Scholar
Strimmer, K, and von Haeseler, A Quartet puzzling. a quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, (1996). 964 969.Google Scholar
Taberlet, P, Waits, L, and Luikart, G Noninvasive genetic sampling: look before you leap. TREE 14, (1999). 323 327.Google Scholar
Thomas, R.H, Schaffner, W, Wilson, A.C, and Pääbo, S DNA phylogeny of the extinct marsupial wolf. Nature 340, (1990). 465 467.Google Scholar
Thompson, R.S, Van Devender, T.R, Martin, P.S, Foppe, T.M, and Long, A Shasta ground sloth (Nothrotheriops shastense Hoffstetter) at Shelter Cave, New Mexico: environment, diet and extinction. Quaternary Research 14, (1980). 360 376.Google Scholar
Tonni, E.P, Prado, J.L, Menegaz, A.N, and Salemme, M.C La unidad mamifero (fauna) Lujanense. Proyeccion de la estratigrafia mamaliana al cuaternario de la region pampeana. Ameghiniana 22, (1985). 255 261.Google Scholar
Vasan, S, Zhang, X, Kapurniotu, A, Bernhagen, J, Teichberg, S, Basgen, J, Wagle, D, Shih, D, Terlecky, I, Bucala, R, Cerami, A, Egan, J, and Ulrich, P An agent cleaving glucose-derived protein crosslinks in vitro and in vivo. Nature 382, (1996). 275 278.Google Scholar
Williams, O.B An improved technique for identification of plant fragments in herbivore feces. Journal of Range Management 22, (1969). 51 52.CrossRefGoogle Scholar