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Hyperspecialization in Some South American Endemic Ungulates Revealed by Long Bone Microstructure

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Abstract

Adaptation to aquatic or semi-aquatic habits has been demonstrated in several distantly related mammalian clades worldwide during the Cenozoic, but curiously none has been conclusively evidenced inland for South America although a few South American native ungulates (SANU) have been proposed as possible subaquatic taxa. These taxa mostly correspond to large-sized herbivorous forms among astrapotheres, pyrotheres, and some toxodontid notoungulates, found at the end of the Paleogene and/or beginning of the Neogene. As no clear argument was provided for these ecological hypotheses, an analysis of the microanatomical features of long bones of some of these taxa in a comparative context was conducted in order to address the question of the paleoecology of these organisms. Our study highlights a variety of osseous specializations in the stylopod bones of SANU, and notably that Parastrapotherium, Pyrotherium, and Nesodon are affected by bone mass increase. If the microanatomical features of Parastrapotherium and Nesodon evoke what is observed in some terrestrial or semi-aquatic graviportal taxa, the very high compactness of Pyrotherium suggests extreme functional requirements in this taxon such as a graviportal hyperspecialization. This study thus evidences the occurrence of several convergent adaptations to graviportality and/or subaquatic habits within SANU and contributes to an important step towards a better integration of South American endemic mammals in large-scaled paleoecological studies.

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Abbreviations

SANU:

South American endemic native ungulates

References

  • Ameghino F (1897) Mammifères crétacés de 1’Argentine. (Deuxième contribution à la connaissance de la faune mammalogique des couches à Pyrotherium). Bol Inst Geogr Argentina Buenos Aires 18:406–429,431–521

    Google Scholar 

  • Avilla LDS, Vizcaíno SF (2005) Locomotory pattern of Astrapotherium magnum (Owen) (Mammalia: Astrapotheria) from the Neomiocene (Colhuehuapian–Santacrucian) of Argentina. II Congresso Latino-Americano de Paleontologia de Vertebrados, Boletim de Resumos, p 44

  • Bellosi ES (2010) Loessic and fluvial sedimentation in Sarmiento Formation pyroclastics, middle Cenozoic of central Patagonia. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 278–292

    Google Scholar 

  • Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166.

    Article  PubMed  PubMed Central  Google Scholar 

  • Billet G (2010) New observations on the skull of Pyrotherium (Pyrotheria, Mammalia) and new phylogenetic hypotheses on South American ungulates. J Mammal Evol 17: 21–59

    Article  Google Scholar 

  • Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  • Boisserie J-R, Fisher RE, Lihoreau F, Weston EM (2011) Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea, Cetancodonta, Cetartiodactyla). Biol Rev 86:601–625

    Article  PubMed  Google Scholar 

  • Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc 100:384–406

    Article  Google Scholar 

  • Carlson KJ, Stout D, Jashashvili T, De Ruiter DJ, Tafforeau P, Carlson K, Berger LR (2011) The endocast of MH1, Australopithecus sediba. Science 333:1402–1407

    Article  CAS  PubMed  Google Scholar 

  • Cassini GH, Cerdeño E, Villafañe AL, Muñoz NA (2012b) Paleobiology of Santacrucian native ungulates (Meridiungulata: Astrapotheria, Litopterna, and Notoungulata). In: Vizcaíno SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia: High-Latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 243–286

    Chapter  Google Scholar 

  • Cassini GH, Vizcaíno S, Bargo M (2012a) Body mass estimation in early Miocene native South American ungulates: a predictive equation based on 3D landmarks. J Zool 287:53–64

    Article  Google Scholar 

  • Charles C, Solé F, Rodrigues HG, Viriot L (2013) Under pressure? Dental adaptations to termitophagy and vermivory among mammals. Evolution 67:1792–1804

    Article  PubMed  Google Scholar 

  • Coombs WP (1975) Sauropod habits and habitats. Palaeogeogr Palaeoclimatol Palaeoecol 17:1–33

    Article  Google Scholar 

  • Cifelli RL (1985) South American ungulate evolution and extinction. In: Stehli FG, Webb SD (eds) The Great American Biotic Interchange. Topics in Geobiology. Plenum Press, New York, pp 249–266.

  • Cornette R, Herrel A, Stoetzel E, Moulin S, Hutterer R, Denys C, Baylac M (2015) Specific information levels in relation to fragmentation patterns of shrew mandibles: do fragments tell the same story? J Archaeol Sci 53:323–330

    Article  Google Scholar 

  • Croft DA (2001) Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Divers Distrib 7:271–287

    Article  Google Scholar 

  • Croft DA, Radic JP, Zurita E, Charrier R, Flynn JJ, Wyss AR (2003) A Miocene toxodontid (Mammalia: Notoungulata) from the sedimentary series of the Cura-Mallín Formation, Lonquimay, Chile. Revista Geológica de Chile 30:285–298

  • Domning DP (1997) Sirenia. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, DC, pp 383–391

  • Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079

    Article  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fish FE (2001) A mechanism for evolutionary transition in swimming mode by mammals. In: Mazin JM, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 261–282

  • Flynn J, Charrier R, Croft D, Wyss A (2012) Cenozoic Andean faunas: shedding new light on South American mammal evolution, biogeography, environments, and tectonics. In: Patterson BD, Costa LP (eds) Bones, Clones, and Biomes: the History and Geography of Recent Neotropical Mammals. The University of Chicago Press, Chicago and London, pp 51–75

  • Forasiepi AM, Cerdeño E, Bond M, Schmidt GI, Naipauer M, Straehl FR, Martinelli AG, Garrido AC, Schmitz MD, Crowley JL (2014) New toxodontid (Notoungulata) from the early Miocene of Mendoza, Argentina. Paläontol Z 89: 611–634

    Article  Google Scholar 

  • Gaudry A (1909) Fossiles de Patagonie: le Pyrotherium. Masson, Paris, pp 1–28

    Google Scholar 

  • Germain D, Laurin M (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool Scr 34:335–350

    Article  Google Scholar 

  • Gheerbrant E, Tassy P (2009) L’origine et l’évolution des éléphants. CR Palevol 8:281–294.

    Article  Google Scholar 

  • Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Mol Phylogenet Evol 40:101–117

    Article  CAS  PubMed  Google Scholar 

  • Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23:458–461

    Article  Google Scholar 

  • Goillot C, Antoine P-O, Tejada J, Pujos F, Gismondi RS (2011) Middle Miocene Uruguaytheriinae (Mammalia, Astrapotheria) from Peruvian Amazonia and a review of the astrapotheriid fossil record in northern South America. Geodiversitas 33:331–345

    Article  Google Scholar 

  • Harmon LJ, Kolbe JJ, Cheverud JM, Losos JB (2005) Convergence and the multidimensional niche. Evolution 59:409–421

    Article  PubMed  Google Scholar 

  • Hayashi S, Carpenter K, Scheyer TM, Watabe M, Suzuki D (2010) Function and evolution of ankylosaur dermal armor. Acta Palaeontol Pol 55:213–228

    Article  Google Scholar 

  • Hayashi S, Houssaye A, Nakajima Y, Chiba K, Ando T, Sawamura H, Inuzuka N, Kaneko N, Osaki T (2013) Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS ONE 8:e59146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integr Zool 4:325–340

    Article  PubMed  Google Scholar 

  • Houssaye A, Lindgren J, Pellegrini R, Lee AH, Germain D, Polcyn MJ (2013) Microanatomical and histological features in the long bones of mosasaurine mosasaurs (Reptilia, Squamata)–implications for aquatic adaptation and growth rates. PloS ONE 8:e76741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houssaye A, Scheyer TM, Kolb C, Fischer V, Sander PM (2014) A new look at ichthyosaur long bone microanatomy and histology: implications for their adaptation to an aquatic life. PLoS ONE 9:e95637

    Article  PubMed  PubMed Central  Google Scholar 

  • Houssaye A., Tafforeau P, Muizon C de, Gingerich PD (2015) Transition of Eocene whales from land to sea: evidence from bone microstructure. PloS ONE 10: e0118409

  • Houssaye A, Waskow K, Hayashi S, Cornette R, Lee AH, Hutchinson JR (In press) Biomechanical evolution of solid bones in large animals: a microanatomical investigation. Biol J Linn Soc

  • Johnson SC, Madden RH (1997) Uruguaytheriine astrapotheres of tropical South America. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, DC, pp 355–382

    Google Scholar 

  • Kay RF, MacFadden BJ, Madden RH, Sandeman H, Anaya F (1998) Revised age of the Salla beds, Bolivia, and its bearing on the age of the Deseadan South American Land Mammal “Age.” J Vertebr Paleontol 18:189–199

    Article  Google Scholar 

  • Kay RF, Williams BA, Anaya F (2002) The adaptations of Branisella boliviana, the earliest South American monkey. In: Plavcan JM, Kay RF, Jungers WL, van Schaik CP (eds) Reconstructing Behavior in the Primate Fossil Record. Kluwer Academic/Plenum Publishers, New York, pp 339–370

    Chapter  Google Scholar 

  • Klein N, Houssaye A, Neenan JM, Scheyer TM (2015) Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia). Contrib Zool 84:59–84

    Google Scholar 

  • Kramarz AG, Bond M (2008) Revisión de Parastrapotherium (Mammalia, Astrapotheria) y otros astrapoterios Deseadenses de Patagonia. Ameghiniana 45:537–551

    Google Scholar 

  • Kramarz A, Bond M (2011) A new early Miocene astrapotheriid (Mammalia, Astrapotheria) from northern Patagonia, Argentina. Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen 260:277–287

    Article  Google Scholar 

  • Kramarz AG, Bond M, Forasiepi AM (2011) New remains of Astraponotus (Mammalia, Astrapotheria) and considerations on astrapothere cranial evolution. Paläontol Z 85:185–200

    Article  Google Scholar 

  • Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M (2008) Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. J Evol Biol 21:807–826

    Article  CAS  PubMed  Google Scholar 

  • Laurin M, Girondot M, Loth M-M (2004) The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30:589–613

    Article  Google Scholar 

  • Lavocat R (1958) Classification des ongulés d’après leur origine et leur évolution. Mammalia 22:28–44

    Article  Google Scholar 

  • Loomis FB (1914) The Deseado Formation of Patagonia. Amherst College, Amherst, 232pp

  • MacFadden BJ (2005) Diet and habitat of toxodont megaherbivores (Mammalia, Notoungulata) from the late Quaternary of South and Central America. Quaternary Res 64:113–124

    Article  Google Scholar 

  • MacFadden BJ (2006) Extinct mammalian biodiversity of the ancient New World tropics. Trends Ecol Evol 21:157–165

    Article  PubMed  Google Scholar 

  • MacFadden BJ, Shockey BJ (1997) Ancient feeding ecology and niche differentiation of Pleistocene mammalian herbivores from Tarija, Bolivia: morphological and isotopic evidence. Paleobiology 23:77–100

    Article  Google Scholar 

  • MacFadden BJ, Campbell Jr, KE, Cifelli RL, Siles O, Johnson NM, Naeser CW, Zeitler PK (1985) Magnetic polarity stratigraphy and mammalian fauna of the Deseadan (late Oligocene-early Miocene) Salla beds of northern Bolivia. J Geol 223–250

  • Marshall LG, Salinas P, Suárez M (1990) Astrapotherium sp.(Mammalia, Astrapotheriidae) from Miocene strata along the Quepuca River, central Chile. Rev Geol Chile, 17:215–223

  • McKenna MC, Bell SK (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York, 631pp

    Google Scholar 

  • Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T (2011) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334:521–524

    Article  CAS  PubMed  Google Scholar 

  • Miquel SE, Bellosi ES (2010) Middle Eocene–Oligocene gastropods of the Sarmiento Formation, central Patagonia. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 61–68

    Google Scholar 

  • Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J (2014) The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater At 324:41–48

    Article  CAS  Google Scholar 

  • Muizon C de, McDonald HG (1995) An aquatic sloth from the Pliocene of Peru. Nature 375:224–227

  • Nakajima Y, Hirayama R, Endo H (2014) Turtle humeral microanatomy and its relationship to lifestyle. Biol J Linn Soc 112:719–734.

    Article  Google Scholar 

  • Nowak RM (1999). Walker’s Mammals of the World (Vol. 2), 6th Edition. The Johns Hopkins University Press, Baltimore

  • Ortiz-Jaureguizar E, Cladera G (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. J Arid Environ 66:498–532

    Article  Google Scholar 

  • Osborn HF (1929) The Titanotheres of Ancient Wyoming, Dakota, and Nebraska. Government Printing Office, Washington, pp 1–953

  • Palazzesi L, Barreda V (2012) Fossil pollen records reveal a late rise of open-habitat ecosystems in Patagonia. Nat Commun 3:1294

    Article  PubMed  Google Scholar 

  • Pascual R, Jaureguizar EO (1990) Evolving climates and mammal faunas in Cenozoic South America. J Hum Evol 19:23–60

    Article  Google Scholar 

  • Pascual R, Ortiz-Jaureguizar E (2007) The Gondwanan and South American episodes: two major and unrelated moments in the history of the South American mammals. J Mammal Evol 14:75–137

    Article  Google Scholar 

  • Paula Couto C de (1979) Tratado de paleomastozoologia. Academia Brasileira de Ciências, Rio de Janeiro, 590pp

  • Quemeneur S, Buffrénil V de, Laurin M (2013) Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol J Linn Soc 109:644–655

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Reguero MA, Prevosti FJ (2010) Rodent-like notoungulates (Typotheria) from Gran Barranca, Chubut Province, Argentina: phylogeny and systematics. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 148–165

    Google Scholar 

  • Ricqlès A de, Buffrénil V de (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin JM, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 289–310

  • Riggs ES (1935) A skeleton of Astrapotherium. Geol Ser Field Mus Nat Hist 6:167–176

  • Salas R, Sánchez J, Chacaltana C (2006) A new pre-Deseadan pyrothere (Mammalia) from northern Peru and the wear facets of molariform teeth of Pyrotheria. J Vertebr Paleontol 26:760–769

    Article  Google Scholar 

  • Sanchez S, Fernandez V, Pierce SE, Tafforeau P (2013) Homogenization of sample absorption for the imaging of large and dense fossils with synchrotron microtomography. Nat Protoc 8:1708–1717

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Villagra MR, Aguilera O, Horovitz I (2003) The anatomy of the world’s largest extinct rodent. Science 301:1708–1710

    Article  PubMed  Google Scholar 

  • Sánchez-Villagra MR, Asher RJ, Rincón AD, Carlini AA, Meylan P, Purdy AW (2004) New faunal reports for the Cerro La Cruz locality (lower Miocene), north-western Venezuela. In: Sánchez-Villagra MR, Clack JA (eds) Fossils of the Miocene Castillo Formation, Venezuela: Contributions in Neotropical Palaeontology. The Palaeontological Society, Special Papers in Palaeontology No. 71, pp. 105–112

  • Scott WB (1913) Land Mammals in the Western Hemisphere. Macmillan, New York, 786pp

    Google Scholar 

  • Scott WB (1937) The Astrapotheria. Proc Am Phil Soc 77:309–393

    Google Scholar 

  • Sefve I (1923) Macrauchenia patagonica. Bull Geol Inst Univ Upsala 19:1–21

    Google Scholar 

  • Shockey BJ (1999) Postcranial osteology and functional morphology of the Litopterna of Salla, Bolivia (late Oligocene). J Vertebr Paleontol 19:383–390

    Article  Google Scholar 

  • Shockey BJ (2001) Specialized knee joints in some extinct, endemic, South American herbivores. Acta Palaeontol Pol 46:277–288

    Google Scholar 

  • Shockey BJ (2005) New leontiniids (Class Mammalia, Order Notoungulata, Family Leontiniidae) from the Salla Beds of Bolivia (Deseadan, late Oligocene). Bull Florida Mus Nat Hist 45:249–260

    Google Scholar 

  • Shockey BJ, Anaya F (2008) Postcranial osteology of mammals from Salla, Bolivia (late Oligocene): form, function, and phylogenetic implications. In: Sargis EJ, Dagosto M (eds) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Springer, Dordrecht, pp 135–157

    Chapter  Google Scholar 

  • Shockey BJ, Anaya FD (2004) Pyrotherium macfaddeni, sp. nov. (late Oligocene, Bolivia) and the pedal morphology of pyrotheres. J Vertebr Paleontol 24:481–488

    Article  Google Scholar 

  • Simpson GG (1980) Splendid Isolation: The Curious History of South American Mammals. Yale University Press, New Heaven, 266pp

    Google Scholar 

  • Steiner CC, Ryder OA (2011) Molecular phylogeny and evolution of the Perissodactyla. Zool J Linn Soc 163:1289–1303

    Article  Google Scholar 

  • Strömberg CA, Dunn RE, Madden RH, Kohn MJ, Carlini AA (2013) Decoupling the spread of grasslands from the evolution of grazer-type herbivores in South America. Nat Commun 4:1478

    Article  PubMed  Google Scholar 

  • Todd NE (2010) New phylogenetic analysis of the family elephantidae based on cranial-dental morphology. Anat Rec 293:74–90

    Article  Google Scholar 

  • Uhen MD (2010) The origin(s) of whales. Annu Rev Earth Planet Sci 38:189–219

    Article  CAS  Google Scholar 

  • Veron G, Patterson BD, Reeves R (2008) Global diversity of mammals (Mammalia) in freshwater. Hydrobiologia 595:607–617

    Article  Google Scholar 

  • Vizcaíno SF, Bargo MS, Kay RF, Fariña RA, Di Giacomo M, Perry JM, Prevosti FJ, Toledo N, Cassini GH, Fernicola JC (2010) A baseline paleoecological study for the Santa Cruz Formation (late–early Miocene) at the Atlantic coast of Patagonia, Argentina. Palaeogeogr Palaeoclimatol Palaeoecol 292:507–519

    Article  Google Scholar 

  • Vizcaíno SF, Cassini GH, Toledo N, Bargo MS (2012) On the evolution of large size in mammalian herbivores of Cenozoic. In: Patterson BP, Costa LP (eds) Bones, Clones and Biomes: an 80-million year History of Recent Neotropical Mammals. The University of Chicago Press, Chicago and London, pp 76–101

  • Vucetich GM, Deschamps CM, Vieytes EC, Montalvo CI (2014) Late Miocene capybaras from Argentina: skull anatomy, taxonomy, evolution, and biochronology. Acta Palaeontol Pol 59:517–535

    Google Scholar 

  • Walker A, Ryan TM, Silcox MT, Simons EL, Spoor F (2008) The semicircular canal system and locomotion: the case of extinct lemuroids and lorisoids. Evol Anthropol Issues News Rev 17:135–145

    Article  Google Scholar 

  • Webb SD (1978). A history of savanna vertebrates in the New World. Part II: South America and the Great Interchange. Annu Rev Ecol Syst 9:393–426

    Article  Google Scholar 

  • Welker CA, Souza-Chies TT, Longhi-Wagner HM, Peichoto MC, McKain MR, Kellogg EA (2015) Phylogenetic analysis of Saccharum sl (Poaceae; Andropogoneae), with emphasis on the circumscription of the South American species. Am J Bot 102:248–263

    Article  PubMed  Google Scholar 

  • Weston EM, Madden RH, Sánchez-Villagra MR (2004) Early Miocene astrapotheres (Mammalia) from northern South America. In: Sánchez-Villagra MR, Clack JA (eds) Fossils of the Miocene Castillo Formation, Venezuela: Contributions on Neotropical Palaeontology. The Palaeontological Society, Special Papers in Palaeontology, No. 71, pp 81–97

  • Wilf P, Cúneo NR, Escapa IH, Pol D, Woodburne MO (2013) Splendid and seldom isolated: the paleobiogeography of Patagonia. Annu Rev Earth Planet Sci 41:561

    Article  CAS  Google Scholar 

  • Williams TM, Worthy GA (2002) Anatomy and physiology: the challenge of aquatic living. In: Hoelzel AR (ed) Marine Mammal Biology: An Evolutionary Approach. Blackwell Science, Oxford, pp 73–97

    Google Scholar 

  • Woodburne MO, Goin FJ, Bond M, Carlini AA, Gelfo JN, López GM, Iglesias A, Zimicz AN (2014) Paleogene land mammal faunas of South America; a response to global climatic changes and indigenous floral diversity. J Mammal Evol 21:1–73

    Article  Google Scholar 

  • Wroe S, Chamoli U, Parr W, Clausen P, Ridgely R, Evans AR (2013) Comparative biomechanical modeling of metatherian and placental saber-tooths: a. different kind of bite for an extreme pouched predator. PLoS ONE 8(6):e66888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We warmly thank C. Lefèvre, J. Lesur, V. Pernègre, and C. Argot (Muséum national d’Histoire naturelle, Paris, France), C. Norris, D. Brinkman, and M. Fox (Yale Peabody Museum, New Haven, USA) for the loan and packing of specimens, J.R. Hutchinson (Royal Veterinary College, London, United Kingdom) for the loan of some scans, Y Nakajima (Bonn Universität, Germany) for the loan of some sections, A. Kramarz (Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina) for helpful comments on astrapothere temporal distribution, and R. Cornette for fruitful advice with statistics. We thank the Steinmann Institut (University of Bonn, Germany) and the ESRF (Grenoble, France) for providing beamtime and support, the ESRF in the framework of the proposal ES-223 on the beamline ID17, UMS 2700 outils et méthodes de la systématique integrative CNRS-MNHN and AST-RX, Plateau technique d’accès scientifique à la tomographie à rayons X du MNHN, M. García-Sanz for performing the scans and reconstructions at the AST-RX platform (MNHN, Paris, France), P. Tafforeau for his help while performing the scans at the ESRF, and UMR 7207 CR2P MNHN CNRS UPMC-Paris6 for 3D imaging facilities. We warmly thank H. Woodward (Oklahoma State University, USA) and an anonymous reviewer for fruitful comments that improved our manuscript, and J.R. Wible for editorial work. A.H. acknowledges financial support from the ANR-13-PDOC-001 and the A. v. Humboldt Foundation.

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AH and G.B designed the study. AH, GB and VF participated to the data acquisition. AH conducted the analyses. AH and GB drafted the manuscript. All authors contributed to the final manuscript, read it and approved it.

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Houssaye, A., Fernandez, V. & Billet, G. Hyperspecialization in Some South American Endemic Ungulates Revealed by Long Bone Microstructure. J Mammal Evol 23, 221–235 (2016). https://doi.org/10.1007/s10914-015-9312-y

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