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First Digital Cranial Endocasts of late Oligocene Notohippidae (Notoungulata): Implications for Endemic South American Ungulates Brain Evolution

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Abstract

Notohippidae were middle-sized toxodonts recorded from the Eocene to the early Miocene. We provide the first description of the cranial endocasts of Rhynchippus equinus and Eurygenium latirostris based on three-dimensional reconstructions extracted from high-resolution X-ray computed tomography imagery. The endocasts of R. equinus and E. latirostris indicate that they were similar in size, proportions of the encephalic components, and neocortical design. The endocranial morphology of these notohippids is very close to that of toxodontids Adinotherium and Nesodon and differs markedly from both other Toxodontia and Typotheria. Notohippids, together with toxodontids, show the most complex neocortical surface among notoungulates. On the other hand, the neuromorphology of notohippids is in contrast to the neocortical morphological pattern described for Tertiary euungulates (Perissodactyla and Artiodactyla) from the Northern Hemisphere and litoptern Protetotheriidae, South American native euungulates. The relative brain size of R. equinus and E. latirostris compared with coeval holarctic euungulates from the late Oligocene are significantly below Perissodactyla and near the values obtained for Artiodactyla. Regarding the location of some functional neocortical areas, the expansion of the frontal lobe in Notohippidae may reflect the acquisition of heightened tactile sensitivity in the front of the snout, as recorded in the somatic sensory cortex of living euungulates. The bulging temporal lobe may reflect expansion of the auditory cortex, likely related to the marked enlargement of the middle ear chamber. Both neuromorphological and quantitative data suggest that during the late Paleogene, notohippids developed as complex and encephalized brains as those of the coeval Artiodactyla of northern continents.

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References

  • Asher RJ, Helgen KM (2010) Nomenclature and placental mammal phylogeny. BMC Evol Biol 10 (1):102

    Article  PubMed Central  PubMed  Google Scholar 

  • Bauchot R, Stephan H (1967) Encéphales et moulages endocraniens de quelques insectivores et primates actuels. In: Problemes actuels in paleontologie (Évolution des Vertébrés): Colloques Interanationaux de Centre National de la Recherche Scientifique. Paris, France, 6–11 June 1966. Editions du Centre National de la Recherché Scientifique 163:575–586

  • Billet G (2011) Phylogeny of the Notoungulata (Mammalia) based on cranial and dental characters. J Syst Palaeontol 9:481–497

    Article  Google Scholar 

  • Billet G, Muizon C de (2013) External and internal anatomy of a petrosal from the late Paleocene of Itaboraí, Brazil, referred to Notoungulata (Placentalia). J Vertebr Paleontol 33:455–469

  • Boddy AM, McGowen MR, Sherwood CC, Grossman LI, Goodman M, Wildman DE (2012) Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling. J Evol Biol 2:981–994

    Article  Google Scholar 

  • Bond M (1986) Los ungulados fósiles de Argentina: evolución y paleoambiente. 4° Congreso argentino de Paleontología y Bioestratigrafía (Mendoza) Actas 2:173–185

  • Brauer K, Schober W (1970) Katalog der Saugetiergehirne. Catalogue of Mammalian Brains. Veb Gustav Fischer Verlag, Jena

    Google Scholar 

  • Cassini GH, Vizcaíno SF, Bargo MS (2012) 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 

  • Cerdeño E, Vera B (2010) Mendozahippus fierensis, gen et sp. nov., new Notohippidae (Notoungulata) from the late Oligocene of Mendoza (Argentina). J Vertebr Paleontol 30:1805–1817

    Article  Google Scholar 

  • Cifelli R (1985) South American ungulate evolution and extinction. In: Stehli F, Wedd S (eds) The Great American Biotic Interchange. Plenum Press, New York, pp 249–266

    Chapter  Google Scholar 

  • Cifelli RL (1993) The phylogeny of the native South American ungulates. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny, Volume 2: Placentals. Springer Verlag, New York, pp 195–216

    Chapter  Google Scholar 

  • Conroy C, Vannier M (1984) Noninvasive three-dimensional computer imaging of matrix-filled fossil skulls by high-resolution computed tomography. Science 226:456–458

    Article  CAS  PubMed  Google Scholar 

  • Dechaseaux C (1958) Encéphales de Notongulés. In: Piveteau J (ed) Traité de Paléontologie. Volume VI. Masson et Cie., Paris, pp 121–129

    Google Scholar 

  • Dechaseaux C (1962) Encéfalos de Notoungulados y de Desdentados Xenartros fósiles. Ameghiniana 2:193–210

    Google Scholar 

  • Dong W (2008) Virtual cranial endocast of the oldest giant panda (Ailuropoda microta) reveals great similarity to that of its extant relative. Naturwissenschaften 95:1079–1083

    Article  CAS  PubMed  Google Scholar 

  • Dozo MT (1987) The endocranial cast of an early Miocene edentate, Hapalops indifferens Ameghino (Mammalia, Edentata, Tardigrada, Megatheriidae). Comparative study with brains of recent sloths. J Hirnforsch 28:397–406

    CAS  PubMed  Google Scholar 

  • Dozo MT (1994) Interpretación del molde endocraneano de Eucholoeops fronto, un Megalonychidae (Mammalia, Xenarthra, Tardigrada) del Mioceno temprano de Patagonia (Argentina). Ameghiniana 31:317–329

    Google Scholar 

  • Dozo MT (1997) Paleoneurología de Dolicavia minuscula (Rodentia, Caviidae) y Paedotherium insigne (Notoungulata, Hegetotheriidae) del Plioceno de Buenos Aires, Argentina. Ameghiniana 34:427–435

    Google Scholar 

  • Dozo MT, Vucetich MG, Candela AM (2004) Skull anatomy and neuromorphology of Hypsosteiromys axiculus, a Colhuehuapian Erethizontidae rodent from Chubut, Argentina. J Vertebr Paleontol 24:228–234

    Article  Google Scholar 

  • Edinger T (1948) Evolution of the horse brain. Geol Soc Am Mem 25:1–177

    Article  Google Scholar 

  • Eisenberg JF (1981) The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation and Behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Elissamburu A (2012) Estimación de la masa corporal en géneros del Orden Notoungulata. Estud Geol (Madr) 68:91–111

    Article  Google Scholar 

  • Feruglio E (1949) Descripción Geológica de la Patagonia. Buenos Aires: Dirección General de Yacimientos Petrolíferos Fiscales II:1–349

  • Gabbert SL (2004) The basicranial and posterior cranial anatomy of the families of the Toxodontia. Bull Am Mus Nat Hist 285:177–190

    Article  Google Scholar 

  • Gervais P (1872) Mémoire sur les formes cérébrales propres à différents groupes de Mammífères. J Zool 1:425–469

    Google Scholar 

  • Jerison HJ (1973) Evolution of the Brain and Intelligence. Academic Press, New York

  • Jerison HJ (1990) Fossil evidence on the evolution of the neocortex. In: Jones EG, Peters A (eds) Cerebral Cortex, Vol. 8A. Plenum Press, New York, pp 285–309

    Google Scholar 

  • Jerison HJ (1991) Fossil, brains and the evolution of the neocortex. In: Finlay BL, Innocenti G, Scheich H (eds) The Neocortex. Ontogeny and Phylogeny. Plenum Press, New York, pp 5–19

    Google Scholar 

  • Johnson JI (1990) Comparative development of somatic sensory cortex. In: Jones EG, Peters A (eds.) Cerebral Cortex, Vol. 8B. Plenum Press, New York, pp 335–449

    Chapter  Google Scholar 

  • Kuhlenbeck H (1978) The Central Nervous System of Vertebrates. Mammalian Telencephalon: Surface Morphology and Central Cortex. The Vertebrate Neuraxis as a Whole. Vol.5, Part II. S. Karger, Basel

  • Loomis FB (1914) The Deseado Formation of Patagonia. Rumford, Concord

    Book  Google Scholar 

  • López GM, Ribeiro AM, Bond M (2010) The Notohippidae (Mammalia, Notoungulata) from Gran Barranca: preliminary considerations. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca. Cambridge University Press, New York, pp 143–151

    Google Scholar 

  • MacPhee RDE (1981) Auditory regions of primates and eutherian insectivores: morphology, ontogeny, and character analysis. Contrib Primatol 18:1–282

  • Macrini TE (2009) Description of a digital cranial endocast of Bathygenys reevesi (Merycoidodontidae; Orodontoidea) and implications for apomorphy-based diagnosis of isolated, natural endocasts. J Vertebr Paleontol 29:1199–1211

    Article  Google Scholar 

  • Macrini TE, Flynn JJ, Croft DA, Wyss AR (2010) Inner ear of a notoungulate placental mammal: anatomical description and examination of potentially phylogenetically informative characters. J Anat 216:600–610

    Article  PubMed Central  PubMed  Google Scholar 

  • Macrini TE, Flynn JJ, Ni X, Croft DA, Wyss AR (2013) Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters. J Anat 223:442–461

    PubMed Central  PubMed  Google Scholar 

  • Macrini TE, Rougier GW, Rowe T (2007) Description of a cranial endocast from the fossil mammal Vincelestes neuquenianus (Theriiformes) and its relevance to the evolution of endocranial characters in therians. Anat Rec 290:875–892

    Article  Google Scholar 

  • Macrini TE, Rowe T, Archer M (2006) Description of a cranial endocast from a fossil platypus, Obdurodon dicksoni (Monotremata, Ornithorhynchidae), and the relevance of endocranial characters to monotreme monophyly. J Morphol 267:1000–1015

    Article  PubMed  Google Scholar 

  • Madden RH (1990) Miocene Toxodontidae (Notoungulata, Mammalia) from Colombia, Ecuador and Chile. Dissertation, Duke University, Durham

  • Marani H, Dozo MT (2005) Nuevos ejemplares de Rhynchippinae (Notoungulata, Notohippidae) de Edad Deseadense (Oligoceno tardío) del Chubut (Argentina): Sistemática y filogenia. Ameghiniana 42 Suplemento:73R

  • Marani H, Dozo MT (2008) El cráneo más completo de Eurygenium latirostris Ameghino, 1895 (Mammalia, Notoungulata), un Notohippidae del Deseadense (Oligoceno Tardío) de la Patagonia, Argentina. Ameghiniana 45:619–626

    Google Scholar 

  • Mendoza M, Janis C, Palmqvist P (2006) Estimating the body mass of extinct ungulates: a study on the use of multiple regression. J Zool 270:90–101

    Google Scholar 

  • Orliac MJ, Argot C, Gilissen E (2012) Digital cranial endocast of Hyopsodus (Mammalia, Condylarthra): a case of Paleogene terrestrial echolocation? PLoS ONE 7 e30000:1–10

    Google Scholar 

  • Orliac MJ, Gilissen E (2012) Virtual endocranial cast of earliest Eocene Diacodexis (Artiodactyla, Mammalia) and morphological diversity of early artiodactyls brains. Proc R Soc B 279:3670–3677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Palombo MR, Kohler M, Moya Sola S, Giovinazzo C (2008) Brain versus body mass in endemic ruminant artiodactyls: a case studied of Myotragus balearicus and smallest Candiacervus species from Mediterranean Islands. Quaternary Internatl 182:160–183

    Article  Google Scholar 

  • Patterson B (1937) Some notoungulates braincasts. Field Mus Nat Hist Geol Ser 6:273–301

    Google Scholar 

  • Patterson B, Pascual R (1972) The fossil mammal fauna of South America. In: Keast A, Erk FC, Glass B (eds) Evolution, Mammals, and Southern Continents. State University of New York Press, Albany, pp 247–309

    Google Scholar 

  • Quiroga JC (1988) Cuantificación de la corteza cerebral en moldes endocraneanos de mamíferos girencéfalos. Procedimiento y aplicación en tres mamíferos extinguidos. Ameghiniana 25:67–84

    Google Scholar 

  • Radinsky L (1968) A new approach to mammalian cranial analysis, illustrated by examples of prosimian primates. J Morphol 124:167–180

    Article  CAS  PubMed  Google Scholar 

  • Radinsky L (1973) Evolution of the canid brain. Brain Behav Evol 7:169–202

    Article  CAS  PubMed  Google Scholar 

  • Radinsky L (1975) Evolution of the felid brain. Brain Behav Evol 11:214–254

    Article  CAS  PubMed  Google Scholar 

  • Radinsky L (1978) Evolution of brain size in carnivores and ungulates. Am Nat 112:815–831

    Article  Google Scholar 

  • Radinsky L (1981) Brain evolution in extinct South American ungulates. Brain Behav Evol 18:169–187

    Article  CAS  PubMed  Google Scholar 

  • Reguero MA, Escribano V (1996) Trachytherus spegazzinianus Ameghino, 1889 (Notoungulata, Mesotheridae) de la edad Deseadense (Oligoceno superior-Mioceno inferior) de Argentina y Bolivia. Naturalia Patagónica, Ciencias de la Tierra 4:43–71

    Google Scholar 

  • Reig O (1981) Teoría del origen y desarrollo de la fauna de mamíferos de América del Sur. Museo Municipal de Ciencias Naturales Lorenzo Scaglia, Monografie Naturae 1:1–162

    Google Scholar 

  • Reperant J (1971) Morphologie compareé de l’encéphale et du moulage endocranien chez les Tylopodes actuels (Mammiferes, Artiodactyles). Bull Mus Natl Hist Nat (3° série) Zool 4:185–321

  • Rowe TB, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332:955–957

  • Sciutto JC, Césari O, Escribano V, Pezzuchi H (2000) Hoja Geológica 4566 III Comodoro Rivadavia, Provincia del Chubut. Servicio Minero Argentino, Instituto de Geología y Recursos Minerales. Boletín N° 244

  • Shockey B (1997) Two new notoungulates (Family Notohippidae) from the Salla beds of Bolivia (Deseadan: late Oligocene): Systematics and functional morphology. J Vertebr Paleontol 17:584–599

    Article  Google Scholar 

  • Shockey BJ, Flynn JJ, Croft DA, Gans P, Wyss AR (2012) New leontiniid Notoungulata (Mammalia) from Chile and Argentina: comparative anatomy, character analysis, and phylogenetic hypotheses. Am Mus Novitates 3737:1–64

    Article  Google Scholar 

  • Shockey BJ, Salas Gismondi R, Gans P, Jeong A, Flynn JJ (2009) Paleontology and geochronology of the Deseadan (late Oligocene) of Moquegua, Perú. Am Mus Novitates 3668:1–24

    Article  Google Scholar 

  • Silcox MT, Dalmyn CK, Hrenchuk A, Bloch JI, Boyer DM, Houde P (2011) Endocranial morphology of Labidolemur kayi (Apatemyidae, Apatotheria) and its relevance to the study of brain evolution in Euarchontoglires. J Vertebr Paleontol 31:1314–1325

    Article  Google Scholar 

  • Simpson GG (1932) Skulls and brains of some mammals from the Notostylops beds of Patagonia. Am Mus Novitates 578:1–11

    Google Scholar 

  • Simpson GG (1933a) Braincasts of Phenacodus, Notostylops and Rhyphodon. Am Mus Novitates 622:1–19

    Google Scholar 

  • Simpson GG (1933b) Braincasts of two typotheres and a litoptern. Am Mus Novitates 629:1–18

    Google Scholar 

  • Simpson GG (1940) The names Mesotherium and Typotherium. Am J Sci 238:518–521

    Article  Google Scholar 

  • Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85:1–350

    Google Scholar 

  • Sutton MD (2008) Tomographic techniques for the study of exceptionally preserved fossils. Proc R Soc B 275:1587–1593

    Article  PubMed Central  PubMed  Google Scholar 

  • Welker F, Collins MJ, Thomas JA, Wadsley M, Brace S, Cappellini C, Turvey ST, Reguero M, Gelfo JN, Kramarz A, Burger J, Thomas-Oates J, Ashford DA, Ashton PD, Rowsell K, Porter DM, Kessler B, Fischer R, Baessmann C, Kaspar S, Olsen JV, Kiley P, Elliott JA, Kelstrup CD, Mullin V, Hofreiter M Willerslev E, Hublin J-J, Orlando L, Barnes I, MacPhee RDE (2015) Ancient proteins resolve the evolutionary history of Darwin’s South American ungulates. Nature doi:10.1038/nature14249

    PubMed  Google Scholar 

  • Welker WI (1990) Why does cerebral cortex fissure and fold? A review of determinants of gyri and sulci. In: Jones EG, Peters A (eds) Cerebral Cortex, Vol. 8B. Plenum Press, New York, pp 3–136

    Chapter  Google Scholar 

  • Welker WI, Adrian HO, Lifschitz W, Kaulen R, Caviedes E, Gutman W (1976) Somatic sensory cortex of llama (Lama glama). Brain Behav Evol 13:284–293.

    Article  CAS  PubMed  Google Scholar 

  • Witmer LM, Ridgely RC, Dufeau DL, Semones MC (2008) Using CT to peer into the past: 3D visualization of the brain and ear regions of birds, crocodiles, and non-avian dinosaurs. In: Endo F, Frey R (eds) Anatomical Imaging: Towards a New Morphology. Springer, New York, pp 67–87

    Chapter  Google Scholar 

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Acknowledgments

The field work upon which this study was based involved the efforts of many people, including J. Fleagle (Stony Brook University), T. Bown (Erathem-Vanir Geological), R. Taylor (Centro Nacional Patagónico), A. Monti (Universidad Nacional de la Patagonia), R. Vacca (Museo Paleontológico Egidio Feruglio), E. Ruigomez (Museo Paleontológico Egidio Feruglio), and M. Tejedor (Centro Nacional Patagónico). We express our gratitude to A. Venter and family (Estancia El Molino owners) for their hospitality during the field work. We also thank L. Reiner (Museo Paleontológico Egidio Feruglio) for the preparation of the artificial endocast and the CT technologist A. Panes (Instituto de Diagnóstico del Este del Chubut) for guidance and help during the scanning and reconstruction processes. W. Simpson (FMNH) permitted study of the L. Radinsky collection of recent and fossil endocranial casts. Finally, we thank the Editor-in-Chief J. R. Wible and two anonymous reviewers who provided careful reviews that improved the manuscript. This research was conducted under permits from Secretaria de Cultura, Chubut Province, Argentina. It was supported by CONICET PIP 2628 and PICT-SECYT 07/32344.

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Correspondence to María Teresa Dozo.

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Dozo, M.T., Martínez, G. First Digital Cranial Endocasts of late Oligocene Notohippidae (Notoungulata): Implications for Endemic South American Ungulates Brain Evolution. J Mammal Evol 23, 1–16 (2016). https://doi.org/10.1007/s10914-015-9298-5

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