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Testing a developmental model in the fossil record: molar proportions in South American ungulates

Published online by Cambridge University Press:  08 April 2016

Laura A. B. Wilson
Affiliation:
Paläontologisches Institut und Museum, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland. E-mail: [email protected]
Richard H. Madden
Affiliation:
Duke University, Department of Biological Anthropology and Anatomy, Duke University Medical Center, Durham, North Carolina 27710, U.S.A.
Richard F. Kay
Affiliation:
Duke University, Department of Evolutionary Anthropology, Durham, North Carolina 27708, U.S.A., and Nicholas School Faculty, Department of Earth and Ocean Sciences, Durham, North Carolina 27708, U.S.A.
Marcelo R. Sánchez-Villagra
Affiliation:
Paläontologisches Institut und Museum, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland. E-mail: [email protected]

Abstract

A developmental model, based upon murine rodents, has been proposed by Kavanagh et al. (2007) to explain lower molar proportions in mammals. We produce a clade-wide macroevolutionary test of the model using the dental evolutionary trends in a unique radiation of extinct mammals endemic to South America (“Meridiungulata”) that comprise a diverse array of molar morphologies. All of the South American ungulate groups examined follow the inhibitory cascade model with the exception of two groups: Interatheriidae (Notoungulata) and Astrapotheria. For most taxa studied, ratios between lower molar areas are greater than 1.0, indicating a weak inhibition by m1 on the subsequent molars in the tooth row, and a trend to greater absolute size of the posterior molars. Comparisons of mean ratios between clades indicate that a significant phylogenetic signal can be detected, particularly between the two groups within Notoungulata— Typotheria and Toxodontia. Body mass estimates were found to be significantly correlated with both m3/m1 and m2/m1 ratios, suggesting that the larger body size achieved the weaker inhibition between the lower molars. Molar ratio patterns are examined and discussed in relation to the independent and numerous acquisitions of hypsodonty that are characteristic of dental evolution in “Meridiungulata.”

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Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Agnolin, F. L., and Chimento, N. R. 2011. Afrotherian affinities for endemic South American “ungulates.”. Mammalian Biology 76:101108.Google Scholar
Arnold, S. J. 1992. Constraints on phenotypic evolution. American Naturalist 140:S85S107.Google Scholar
Billet, G. 2010. New observations on the skull of Pyrotherium (Pyrotheria, Mammalia) and new phylogenetic hypotheses on South American ungulates. Journal of Mammalian Evolution 17:2159.Google Scholar
Billet, G., and Martin, T. 2011. No evidence for an afrotherian-like delayed dental eruption in South American notoungulates. Naturwissenschaften 98:509517.Google Scholar
Billet, G., de Muizon, C., and Quispe, B. M. 2008. Late Oligocene mesotheriids (Mammalia, Notoungulata) from Salla and Lacayani (Bolivia): implications for basal mesotheriid phylogeny and distribution. Zoological Journal of the Linnean Society 152:153200.Google Scholar
Billet, G., Blondel, C., and de Muizon, C. 2009. Dental microwear analysis of notoungulates (Mammalia) from Salla (Late Oligocene, Bolivia) and discussion on their precocious hypsodonty. Palaeogeography, Palaeoclimatology, Palaeoecology 274:114124.Google Scholar
Bond, M. 1999. Quaternary native ungulates of southern South America: a synthesis. Quaternary of South American and Antarctic Peninsula 12:177206.Google Scholar
Bond, M., Perea, D., Ubilla, M., and Tauber, A. 2001. Neolicaphrium recens Frenguelli, 1921, the only surviving Proterotheriidae (Litopterna, Mammalia) into the South American Pleistocene. Palaeovertebrata 30:3750.Google Scholar
Cifelli, R. L. 1983. The origin and affinities of the South American Condylarthra and early Tertiary Litopterna (Mammalia). American Museum Novitates 9:149.Google Scholar
Cifelli, R. L. 1985. South American ungulate evolution and extinction. Pp. 249266inStehli, F. G.and Webbs, S. D., eds. The Great American Biotic Interchange. Plenum, New York.Google Scholar
Cifelli, R. L., and Guerrero, J. 1997. Litopterns. Pp. 289302inKay, R. F., Madden, R. H., Cifelli, R. L., and Flynn, J. J., eds. Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, D.C..Google Scholar
Cifelli, R. L., and Soria, M. P. 1983. Systematics of the Adianthidae (Litopterna, Mammalia). American Museum Novitates 2771:125.Google Scholar
Croft, D. A., and Anaya, F. 2006. A new middle Miocene hegetotheriid (Notoungulata; Typotheria) and a phylogeny of the Hegetotheriidae. Journal of Vertebrate Paleontology 26:387399.Google Scholar
Croft, D. A., and Weinstein, D. 2008. The first application of the mesowear method to endemic South American ungulates (Notoungulata). Palaeogeography, Palaeoclimatology, Palaeoecology 269:103114.Google Scholar
Croft, D. A., Bond, M., Flynn, J. J., Reguero, M., and Wyss, A. R. 2003a. Large archaeohyracids (Typotheria, Notoungulata) from Central Chile and Patagonia, including a revision of Archaeotypotherium. Fieldiana Geology 49:138.Google Scholar
Croft, D. A., Radic, J. P., Zurita, E., Charrier, R., Flynn, J. J., and Wyss, A. R. 2003b. A Miocene toxodontid (Mammalia: Notoungulata) from the sedimentary series of the Cura-Mallin Formation, Lonquimay, Chile. Revista Geológica de Chile 30:285298.Google Scholar
Croft, D. A., Flynn, J. J., and Wyss, A. R. 2004. Notoungulata and Litopterna of the early Miocene Chucal fauna, northern Chile. Fieldiana (Geology), new series 50:152.Google Scholar
Damuth, J. 1990. Problems in estimating body masses of archaic ungulates using dental measurements. Pp. 229253inDamuth, J.and MacFadden, B. J., eds. Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge.Google Scholar
De Muizon, C., and Cifelli, R. L. 2000. The “condylarths” (archaic Ungulata, Mammalia) from the early Palaeocene of Tiupampa (Bolivia): implications on the origin of the South American ungulates. Geodiversitas 22:47150.Google Scholar
Elissamburu, A. 2004. Análisis morfométrico y morfofunctional del esqueleto appendicular de Paedotherium (Mammalia, Notoungulata). Ameghiniana 41:2543.Google Scholar
Flynn, J. J., and Wyss, A. R. 1998. Recent advances in South American mammalian paleontology. Trends in Ecology and Evolution 13:449454.Google Scholar
Gingerich, P. D., and Schoeninger, M. J. 1979. Patterns of tooth size variability in the dentitions of primates. American Journal of Physical Anthropology 51:457465.Google Scholar
Greaves, W. S. 1978. The jaw lever system in ungulates: a new model. Journal of Zoology 184:271285.Google Scholar
Greaves, W. S. 1983. A functional analysis of carnassial biting. Biological Journal of the Linnean Society 20:353363.Google Scholar
Janis, C. M. 1988. An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preference. Mémoires, Muséum National d'Histoire Naturelle, Paris, série C 53:367387.Google Scholar
Jarvinen, E., Salazar-Ciudad, I., Birchmeier, W., Taketo, M. M., Jernvall, J., and Thesleff, I. 2006. Continuous tooth generation in mouse is induced by activated epithelial wnt7beta-catenin signaling. Proceedings of the National Academy of Sciences USA 103:1862718632.Google Scholar
Jernvall, J., Keranen, S. V. E., and Thesleff, I. 2000. Evolutionary modification of development in mammalian teeth: quantifying gene expression patterns and topography. Proceedings of the National Academy of Sciences USA 97:1444414448.Google Scholar
Kavanagh, K. D., Evans, A. R., and Jernvall, J. 2007. Predicting evolutionary patterns of mammalian teeth from development. Nature 449:427433.Google Scholar
Kramarz, A. G. 2009. Adiciones al conocimiento de Astrapothericulus (Mammalia, Astrapotheria): anatomía cráneo-dentaria, diversidad y distribuciόn. Revista Brasileira de Paleontologia 12:5566.Google Scholar
Kramarz, A. G., and Bond, M. 2009. A new Oligocene astrapothere (Mammalia, Meridiungulata) from Patagonia and a new appraisal of astrapothere phylogeny. Journal of Systematic Paleontology 7:117128.Google Scholar
Madden, R. H. 1997. A new toxodontid notoungulate. Pp. 355381inKay, R. F., Madden, R. H., Cifelli, R. L., and Flynn, J. J., eds. Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, D.C..Google Scholar
Marshall, L. G., and Cifelli, R. L. 1990. Analysis of changing diversity patterns in Cenozoic land mammal age faunas, South America. Palaeovertebrata 19:169210.Google Scholar
McKenna, M. C. 1975. Toward a phylogenetic classification of mammals. Pp. 2146inLuckett, W. P.and Szalay, F. S., eds. Phylogeny of the primates. Plenum, New York.Google Scholar
McKenna, M. C., and Bell, S. K. 1997. Classification of mammals above the species level. Columbia University Press, New York.Google Scholar
Mendoza, M., and Palmqvist, P. 2008. Hypsodonty in ungulates: an adaptation for grass consumption or for foraging in open habitat? Journal of Zoology 274:134142.Google Scholar
Munne, P. M., Tummers, M., Jarvinen, E., Thesleff, I., and Jernvall, J. 2009. Tinkering with the inductive mesenchyme: Sostdc1 uncovers the role of dental mesenchyme in limiting tooth induction. Development 136:393402.Google Scholar
Oliveira, E. V., and Bergqvist, L. P. 1998. A new Paleocene armadillo (Mammalia, Dasypodoidea) from the Itaboraí Basin, Brazil. InCasadío, S., ed. Paleόgeno de América del Sur y de la Península Antártica. Asociaciόn Paleontolόgica Argentina Publicaciόn Especial 5:3540. Buenos Aires.Google Scholar
Owen, R. 1837. A description of the cranium of Toxodon platensis; a gigantic extinct mammiferous species, referable by its dentition to the Rodentia, but with affinities to the Pachydermata and the herbivorous Cetacea. Proceedings of the Geological Society of London 2:541542.Google Scholar
Owen, R. 1840. A description of the cranium of Toxodon platensis; a gigantic extinct mammiferous animal, referable to the Order Pachydermata, but with affinities to the Rodentia, Edentata, and herbivorous Cetacea. Pp. 1635inDarwin, C., ed. The zoology of the voyage of HMS Beagle, under the command of Captain Fitzroy, RN, during the years 1832–1836, Part 1. Fossil Mammalia. Smith, Elder, London.Google Scholar
Patterson, B., and Pascual, R. 1972. The fossil mammal fauna of South America. Pp. 247309inKeast, A., Erk, F. C., Glass, B., eds. Evolution, mammals, and southern continents. State University of New York Press, Albany.Google Scholar
Paula-Couto, C. 1952. Fossil mammals from the beginning of the Cenozoic in Brazil: Condylarthra, Litopterna, Xenungulata and Astrapotheria. Bulletin of the American Museum of Natural History 99:359394.Google Scholar
Peterson, K. J., Summons, R. E., and Donoghue, P. C. J. 2007. Molecular palaeobiology. Paleontology 50:775809.Google Scholar
Polly, P. D. 1998. Variability in mammalian dentitions: size-related bias in the coefficient of variation. Biological Journal of the Linnean Society 64:8389.Google Scholar
Polly, P. D. 2007. Development with a bite. Nature 229:413415.Google Scholar
Polly, P. D. 2008. Developmental dynamics and G-matrices: can morphometric spaces be used to model phenotypic evolution. Evolutionary Biology 35:8396.CrossRefGoogle Scholar
Reguero, M. A. 1998. El problema de las relaciones sistemáticas y filogenéticas de los Typotheria y Hegetotheria (Mammalia, Notoungulata): análisis de los taxones de Patagonia de la edad-mamífero Deseadense (Oligoceno). Ph.D. thesis. Universidad de Buenos Aires, Buenos Aires.Google Scholar
Reguero, M. A., Candela, A. M., and Cassini, G. H. 2010. Hypsodonty and body size in rodent-like notoungulates. Pp. 362374inMadden, R. H., Carlini, A. A., Vucetich, M. G., and Kay, R. F., eds. The paleontology of Gran Barranca: evolution and environmental change. Cambridge University Press, New York.Google Scholar
Renvoisé, E., Evans, A. R., Jabrane, A., Labruère, C., Laffont, R., and Montuire, S. 2009. Evolution of mammal tooth patterns: new insights from a developmental prediction model. Evolution 63:13271340.Google Scholar
Riggs, D. S., Guarnieri, J. A., and Addelman, S. 1978. Fitting straight lines when both variables are subject to error. Life Sciences 22:13051360.Google Scholar
Salazar-Ciudad, I., and Jernvall, J. 2002. A gene network model accounting for development and evolution of mammalian teeth. Proceedings of the National Academy of Sciences USA 99:81168120.Google Scholar
Salazar-Ciudad, I., and Jernvall, J. 2004. How different types of pattern formation mechanisms affect the evolution of form and development. Evolution and Development 6:616.Google Scholar
Salazar-Ciudad, I., and Jernvall, J. 2010. A computational model of teeth and the developmental origins of morphological variation. Nature 464:583586.Google Scholar
Sánchez-Villagra, M. R. 2010. Developmental paleontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives. Proceedings of the Royal Society of London B 277:11391147.Google Scholar
Scarano, A. C. 2010. El proceso de desarrollo de la hipsodoncia durante la transiciόn Eoceno-Oligoceno: el caso de los ungulados autόctonos del Orden Notoungulata (Mammalia). Ph.D. thesis. Universidad Nacional de La Plata, La Plata, Argentina.Google Scholar
Scherer, C. S., Pitana, V. G., and Ribeiro, A. M. 2009. Proterotheriidae and Macrauchenidae (Litopterna, Mammalia) from the Pleistocene of Rio Grande do Sul State, Brazil. Revista Brasileira de Paleontologia 12:231246.Google Scholar
Scott, W. B. 1937. The Astrapotheria. Proceedings of the American Philosophical Society 77:309393.Google Scholar
Shockey, B. J., Croft, D. A., and Anaya, F. 2007. Analysis of function in the absence of extant functional analogs: a case study of mesotheriid notoungulates. Paleobiology 33:227247.Google Scholar
Simpson, G. G. 1967. The beginning of the age of mammals in South America, Part 2. Bulletin of the American Museum of Natural History 137:1260.Google Scholar
Simpson, G. G. 1980. Splendid isolation: the curious history of South American mammals. Yale University Press, New Haven, Conn.Google Scholar
Townsend, K. E. B., and Croft, D. A. 2008. Diets of notoungulates from the Santa Cruz formations, Argentina: new evidence from enamel microwear. Journal of Vertebrate Paleontology 28:217230.Google Scholar
Vucetich, M. G., Carlini, A. A., Aguilera, O., and Sánchez-Villagra, M. R. 2010. The tropics as reservoir of otherwise extinct mammals: the case of rodents from a new Pliocene faunal assemblage from Northern Venezuela. Journal of Mammalian Evolution 17:265273.Google Scholar
Werdelin, L. 1987. Jaw geometry and molar morphology in marsupial carnivores: analysis of a constraint and its macroevolutionary consequences. Paleobiology 13:342350.Google Scholar
Weston, E. M., Madden, R. H., and Sánchez-Villagra, M. R. 2004. Early Miocene astrapotheres (Mammalia) from northern South America. InSánchez-Villagra, M. R., and Clack, J. A., eds. Fossils of the Miocene Castillo Formation, Venezuela: contributions on Neotropical paleontology. Special Papers in Paleontology. 71:8197. Palaeontological Association, London.Google Scholar
Williams, H. S. H., and Kay, R. 2001. A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution 8:207229.Google Scholar
Wilson, L. A. B., and Sánchez-Villagra, M. R. 2009. Heterochrony and patterns of cranial suture closure in hystricognath rodents. Journal of Anatomy 214:339354.Google Scholar
Wolpoff, M. H. 1985. Tooth size-body scaling in a human population: theory and practice of an allometric analysis. Pp. 273318inJungers, W. L., ed. Size and scaling in primate biology. Plenum, New York.Google Scholar
Woodburne, M. O. 2010. The Great American Biotic Interchange: dispersals, tectonics, climate, sea level and holding pens. Journal of Mammalian Evolution 17:245264.Google Scholar