Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T17:47:06.520Z Has data issue: false hasContentIssue false
  • English
  • Français

Heterochrony, dental ontogenetic diversity, and the circumvention of constraints in marsupial mammals and extinct relatives

Published online by Cambridge University Press:  08 April 2016

Analía M. Forasiepi  and
Marcelo R. Sánchez-Villagra
Analía M. Forasiepi
Affiliation:
CONICET, IANIGLA, CCT-Mendoza, Ruiz Leal s/n, Mendoza 5500, Argentina, and Paläontologisches Institut und Museum, Karl Schmid-Strasse 4, Zürich CH-8006, Switzerland. E-mail: [email protected]
Marcelo R. Sánchez-Villagra
Affiliation:
Paläontologisches Institut und Museum, Karl Schmid-Strasse 4, Zürich CH-8006, Switzerland. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In marsupial mammals and their extinct relatives—collectively, metatherians—only the last premolar is replaced, but the timing of dental eruption is variable within the group. Our knowledge of fossils metatherians is limited, but is critical to understanding several aspects of the evolution and morphological diversification of this clade. We analyzed the sequence of eruption of 76 specimens of metatherians, including Sparassodonta, an extinct clade of specialized carnivores from South America. In Sparassodonta (1) the P3/p3 erupt simultaneously, in common with some didelphids (in other didelphids, p3 erupts before P3, whereas in the remaining didelphids, some peramelids, one caenolestid, and Pucadelphys this order is reversed); (2) the upper and lower molars at the same locus erupt more in synchrony than in other carnivorous metatherians in which the lower molars clearly precede the upper equivalents; (3) the upper canine in thylacosmilids and proborhyaenids is hypselodont; (4) species with similar molar morphologies have different morphologies of the deciduous premolars, suggesting diverse diets among the juveniles of different taxa; (5) deciduous teeth are functional for a long period of time, with thylacosmilids even retaining a functional DP3 in the permanent dentition. The retention of the DP3 and the hypertrophied and hypselodont upper canine of thylacosmilids represent clear heterochronic shifts. Specializations in the timing of dental eruption and in the deciduous tooth shape of sparassodonts are evolutionary mechanisms that circumvent constraints imposed by the metatherian replacement pattern and increase morphological disparity during ontogeny.

Type
Articles
Information
Paleobiology , Volume 40 , Issue 2 , Spring 2014 , pp. 222 - 237
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Anders, U., von Koenigswald, W., Ruf, I., and Smith, B. 2011. Generalized individual dental age stages for fossil and extant placental mammals. Paläontologische Zeitschrift 85:321–339.Google Scholar
Archer, M. 1975. Abnormal dental development and its significance in dasyurids and other marsupials. Memoirs of the Queensland Museum 17:251–265.Google Scholar
Archer, M. 1976. The dasyurid dentition and its relationships to that of didelphids, thylacinids, borhyaenids (Marsupicarnivora) and peramelids (Peramelina: Marsupialia). Australian Journal of Zoology, suppl. series 39:1–34.Google Scholar
Arena, D. A, Archer, M., Godthelp, H., Hand, S. J., and Hocknull, S. 2011. Hammer-toothed “marsupial skinks” from the Australian Cenozoic. Proceedings of the Royal Society of London B 278:3529–3533.Google Scholar
Asher, R. J., and Lehmann, T. 2008. Dental eruption in afrotherian mammals. BMC Biology 6:14.Google Scholar
Astúa, D., and Leiner, N. O. 2008. Tooth eruption sequence and replacement pattern in Woolly Opossums, genus Caluromys (Didelphimorphia: Didelphidae). Journal of Mammalogy 89:244–251.Google Scholar
Babot, M. J., Powell, J. E., and de Muizon, C. 2002. Callistoe vincei, a new Proborhyaenidae (Borhyaenoidea, Metatheria, Mammalia) from the early Eocene of Argentina. Geobios 35:615–629.Google Scholar
Beck, R. M. D., Godthelp, H., Weisbecker, V., Archer, M., and Hand, S. J. 2008. Australia's oldest marsupial fossils and their biogeographical implications. PLoS ONE 3:e1858.Google Scholar
Bennett, C. V., and Goswami, A. 2013. Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biology 11:52.Google Scholar
Bensley, B. A. 1903. On the evolution of the Australian Marsupialia with remarks on the relationships of the marsupials in general. Transactions of the Linnean Society of London (Zoology), 2nd series 9:83–217.Google Scholar
Bond, M., and Pascual, R. 1983. Nuevos y elocuentes restos craneanos de Proborhyaena gigantea Ameghino, 1897 (Marsupialia, Borhyaenidae, Proborhyaeninae) de la Edad Deseadense: un ejemplo de coevolución. Ameghiniana 20:47–60.Google Scholar
Butler, P. M. 1946. The evolution of carnassial dentitions in Mammalia. Journal of Zoology 116:198–220.Google Scholar
Charles, C., Solé, F., Rodrigues, H. G., and Viriot, L. 2013. Under pressure? Dental adaptations to termitophagy and vermivory among mammals. Evolution 67:1792–1804.Google Scholar
Churcher, C. S. 1985. Dental functional morphology in the marsupial sabre-tooth Thylacosmilus atrox (Thylacosmilidae) compared to that of felid sabre-tooths. Australian Mammalogy 8:201–220.Google Scholar
Cifelli, R. L., and de Muizon, C. 1998. Tooth eruption and replacement pattern in early marsupials. Comptes Rendus de l'Académie des Sciences 326:215–220.Google Scholar
Cifelli, R. L., Rowe, T. B., Luckett, W. P., Banta, J., Reyes, R., and Howes, R. I. 1996. Origin of marsupial pattern of tooth replacement: fossil evidence revealed by high resolution X-ray CT. Nature 379:715–718.Google Scholar
Clemens, W. A. 1979. Marsupialia. Pp. 192–220inLillegraven, J. A., Kielan-Jaworowska, Z., and Clemens, W. A., eds. Mesozoic mammals: the first two-thirds of mammalian history. University of California Press, Berkeley.Google Scholar
Clemens, W. A., and Lillegraven, J. A. 1986. New Late Cretaceous North American advance therian mammals that fit neither the marsupial nor eutherian molds. Contributions to Geology, University of Wyoming, Special Paper 3:55–85.Google Scholar
Crompton, A. W. 1971. The origin of the tribosphenic molar. InKermack, D. M. and Kermack, K. A., eds. Early mammals. Zoological Journal of the Linnean Society 50 (Suppl. 1):65–87.Google Scholar
Degrange, F. J., Tambussi, C. P., Moreno, K., Witmer, L. M., and Wroe, S. 2010. Mechanical analysis of feeding behavior in the extinct “terror bird” Andalgalornis steulleti (Gruiformes: Phorusrhacidae). PLoS ONE 5:e1 1856.Google Scholar
Dependorff, T. 1898. Zur Entwickelungsgeschichte des Zahnsystems der Marsupialier. Pp. 244–402inSemon, R. W., ed. Zoologische Forschungsreisen in Australien und dem Malaiischen Archipel, Vol. III. Monotremen und Marsupialier II, Part I. Denkschriften der Medizinisch-Naturwissenschaftliche Gesellschaft zu Jena, Vol. 6 (1897–1901).Google Scholar
Díaz, M. M., and Flores, D. A. 2008. Early reproduction onset in four species of Didelphimorphia in the Peruvian Amazonia. Mammalia 72:126–130.Google Scholar
Ercoli, M. D., Prevosti, F. J., and Forasiepi, A. M. 2013. The structure of the mammalian predator guild in the Santa Cruz Formation (late early Miocene), Patagonia, Argentina. Journal of Mammalian Evolution. doi: 10.1007/s10914-013-9243-4.CrossRefGoogle Scholar
Evans, A. R., Wilson, G. P., Fortelius, M., and Jernvall, J. 2007. High-level similarity of dentitions in carnivorans and rodents. Nature 445:78–81.Google Scholar
Figueirido, B., and Janis, C. M. 2011. The predatory behaviour of the thylacine: Tasmanian tiger or marsupial wolf? Biology Letters 7:937–940.Google Scholar
Flower, W. H. 1867. On the development and succession of the teeth in the Marsupialia. Philosophical Transactions of the Royal Society of London B 157:631–642.Google Scholar
Flower, W. H. 1869. Remarks on the homologies and notation of the teeth of the Mammalia. Journal of Anatomy and Physiology 3:262–278.Google Scholar
Forasiepi, A. M. 2009. Osteology of Arctodictis sinclairi (Mammalia, Metatheria, Sparassodonta) and phylogeny of Cenozoic metatherian carnivores from South America. Monografías del Museo Argentino de Ciencias Naturales, new series 6:1–174.Google Scholar
Forasiepi, A. M., and Carlini, A. A. 2010. New thylacosmilid (Mammalia, Metatheria, Sparassodonta) from the Miocene of Patagonia, Argentina. Zootaxa 2552:55–68.Google Scholar
Giannini, N. P., Abdala, F., and Flores, D. A. 2004. Comparative postnatal ontogeny of the skull in Dromiciops gliroides (Marsupialia: Microbiotheriidae). American Museum Novitates 3460:1–17.Google Scholar
Goin, F. J., and Pascual, R. 1987. News on the biology and taxonomy of the marsupials Thylacosmilidae (late Tertiary of Argentina). Anales de la Academia Nacional de Ciencias Exactas Físicas y Naturales de Buenos Aires 39:219–246.Google Scholar
Goin, F. J., Abello, A., Bellosi, E., Kay, R., Madden, R., and Carlini, A. A. 2007. Los Metatheria sudamericanos de comienzos del Neógeno (Mioceno Temprano, edad-mamífero Colhuehuapense), Parte I. Introducción, Didelphimorphia y Sparassodonta. Ameghiniana 44:29–71.Google Scholar
Goswami, A., Milne, N., and Wroe, S. 2011. Biting through constraints: cranial morphology, disparity, and convergence across living and fossil carnivorous mammals. Proceedings of the Royal Society of London B 278:1831–1839.Google Scholar
Greaves, W. S. 1983. A functional analysis of carnassial biting. Biological Journal of the Linnean Society 20:353–363.Google Scholar
Hillson, S. 2005. Teeth, 2nd ed. Cambridge University Press, Cambridge.Google Scholar
Kielan-Jaworowska, Z., Cifelli, R. L., and Luo, Z. X. 2004. Mammals from the age of dinosaurs: origin, evolution, and structure. Columbia University Press, New York.Google Scholar
Kobayashi, Y., Winkler, D. A., and Jacobs, L. L. 2002. Origins of the tooth-replacement pattern in the therian mammals: evidence from 110 Myr old fossil. Proceedings of the Royal Society of London B 269:369–373.Google Scholar
Luckett, W. P. 1989. Developmental evidence for dental homologies in the marsupial family Dasyuridae. Anatomical Record 223:70A.Google Scholar
Luckett, W. P. 1993. An ontogenetic assessment of dental homologies in therian mammals. Pp. 182–204inSzalay, F. S., Novacek, M. J., and McKenna, M. C., eds. Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials. Springer, New York.Google Scholar
Luckett, W. P., and Hong, N. 2000. Ontogenetic evidence for dental homologies and premolar replacement in fossil and extant caenolestids (Marsupialia). Journal of Mammalian Evolution 7:109–127.Google Scholar
Luckett, W. P., and Woolley, P. A. 1996. Ontogeny and homology of the dentition in dasyurid mammals: development in Sminthopsis virginiae. Journal of Mammalian Evolution 3:327–364.Google Scholar
Luo, Z. X., Kielan-Jaworowska, Z., and Cifelli, R. L. 2004. Evolution of dental replacement in mammals. Bulletin of Carnegie Museum of Natural History 36:159–175.Google Scholar
Marshall, L. G. 1976. Notes on the deciduous dentition of the Borhyaenidae (Marsupialia: Borhyaenoidea). Journal of Mammalogy 57:751–754.Google Scholar
Marshall, L. G. 1978. Evolution of the Borhyaenidae, extinct South American predaceous marsupials. University of California Publications in Geological Sciences 117:1–89.Google Scholar
Marshall, L. G. 1979. Review of the Prothylacyninae, an extinct subfamily of South American “dog-like” marsupials. Fieldiana (Geology), new series 3:1–50.Google Scholar
Marshall, L. G. 1981 Review of the Hathlyacyninae, an extinct subfamily of South American “dog-like” marsupials. Fieldiana Geology, new series 7:1–120.Google Scholar
Marshall, L. G., Case, J. A., and Woodburne, M. O. 1990. Phylogenetic relationships of the families of marsupials. Current Mammalogy 2:433–502.Google Scholar
Martin, G. M. 2005. Intraspecific variation in Lestodelphys halli (Marsupialia: Didelphimorphia). Journal of Mammalogy 86:793–802.Google Scholar
Martin, T. 1997. Tooth replacement in Late Jurassic Dryolestidae (Eupantotheria, Mammalia). Journal of Mammalian Evolution 4:1–18.Google Scholar
McNamara, K. J. 1986. A guide to the nomenclature of heterochrony. Journal of Paleontology 60:4–13.Google Scholar
Muizon, C. de, and Lange-Badré, B. 1997. Carnivorous dental adaptations in tribosphenic mammals and phylogenetic reconstruction. Lethaia 30:351–366.Google Scholar
Nedin, C. 1991. The dietary niche of the extinct Australian marsupial lion: Thylacoleo carnifex Owen. Lethaia 24:115–118.CrossRefGoogle Scholar
O'Leary, M. A. O., Bloch, J. L., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B. P., Luo, Z.-X., Meng, J., Ni, X., Novacek, M. J., Perini, F. A., Randall, Z. S., Rougier, G. W., Sargis, E. J., Silcox, M. T., Simmons, N. B., Spaulding, M., Velazco, P. M., Weksler, M., Wible, J. R., and Cirranello, A. L. 2013 The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339:662–667.Google Scholar
Owen, R. 1845. Odontography; or, a treatise on the comparative anatomy of the teeth; their morphological relations, mode of development, and microscopic structure in vertebrate animals. Hippolyte Baillière, London.Google Scholar
Petrides, G. A. 1949. Sex and age determination in the opossum. Journal of Mammalogy 30:364–378.Google Scholar
Prevosti, F. J., Turazzini, G. F., and Chemisquy, M. A. 2010. Morfología craneana en tigres dientes de sable: alometría función y filogenia. Ameghiniana 47:239–256.Google Scholar
Prevosti, F. J., Turazzini, G. F., Ercoli, M. D., and Hingst-Zaher, E. 2011. Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics. Zoological Journal of the Linnean Society 164:836–855.Google Scholar
Prevosti, F. J., Forasiepi, A. M., and Zimicz, N. 2013. The evolution of the Cenozoic terrestrial mammalian predator guild in South America: competition or replacement? Journal of Mammalian Evolution 20:3–21.Google Scholar
Riggs, E. S. 1934. A new marsupial saber-tooth from the Pliocene of Argentina and its relationships to other South American predaceous marsupials. Transactions of the American Philosophical Society, new series 24:1–31.Google Scholar
Rothecker, J., and Storer, J. E. 1996. The marsupials of the Lac Pelletier Lower Fauna, middle Eocene (Duchesnean) of Saskatchewan. Journal of Vertebrate Paleontology 16:770–774.Google Scholar
Rougier, G. W., Wible, J. R., and Novacek, M. J. 1998. Implications of Deltatheridium specimens for early marsupial history. Nature 396:459–463.Google Scholar
Sánchez-Villagra, M. R. 2002. Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. Journal of Experimental Zoology B 294:264–273.Google Scholar
Sánchez-Villagra, M. R. 2013. Why are there fewer marsupials than placentals? On the relevance of geography and physiology to evolutionary patterns of mammalian diversity and disparity. Journal of Mammalian Evolution. 20:279–290.Google Scholar
Scheyer, T. M., Aguilera, O. A., Delfino, M., Fortier, D. C., Carlini, A. A., Sánchez, R., Carrillo-Briceño, J. D., Quiroz, L., and Sánchez-Villagra, M. R. 2013. Crocodylian diversity peak and extinction in the late Cenozoic of the northern Neotropics. Nature Communications 4:1907. doi: 10.1038/ncomms2940.Google Scholar
Sears, K. E. 2004. Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58:2353–2370.Google Scholar
Simpson, G. G. 1936. Studies on the earliest mammalian dentition. Dental Cosmos 78:791–800.Google Scholar
Simpson, G. G. 1948. The beginning of the age of mammals in South America. Bulletin of the American Museum of Natural History 91:1–232.Google Scholar
Smith, K. K. 2001. Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73:169–186.Google Scholar
Smith, K. K. 2002. Sequence heterochrony and the evolution of development. Journal of Morphology 252:82–97.Google Scholar
Smits, P. D., and Evans, A. R. 2012. Functional constraints on tooth morphology in carnivorous mammals. BMC Evolutionary Biology 12:1–11.Google Scholar
Soibelzon, L. H. 2010. First description of milk teeth of fossil South American procyonid from the lower Chapadmalalan (Late Miocene–Early Pliocene) of “Farola Monte Hermoso,” Argentina: paleoecological considerations. Paläontologische Zeitschrift 85:83–89.Google Scholar
Springer, M. S., Kirsch, J. A. W., and Case, J. A. 1997. The chronicle of marsupial evolution. Pp. 129–161inGivnish, T. and Sytsma, K., eds. Molecular evolution and adaptive radiation. Cambridge University Press, New York.Google Scholar
Tate, G. H. H. 1951. The banded anteater, Myrmecobius Waterhouse (Marsupialia). American Museum Novitates 1521:1–8.Google Scholar
Thomas, O. 1887. On the homologies and succession of the teeth in the Dasyuridae, with an attempt to trace the history of the evolution of mammalian teeth in general. Philosophical Transactions of the Royal Society of London B 178:443–462.Google Scholar
Tribe, C. J. 1990. Dental age classes in Marmosa incana and other didelphoids. Journal of Mammalogy 71:566–569.Google Scholar
Turnbull, W. D. 1971. The Trinity therians: their bearing on evolution in marsupials and other therians. Pp. 151–179inDahlberg, A. A., ed. Dental morphology and evolution. University of Chicago Press, Chicago.Google Scholar
Turnbull, W. D. 1978. Another look at dental specialization in the extinct saber-toothed marsupial, Thylacosmilus, compared with its placental counterparts. Pp. 399–414inButler, P. M. and Joysey, K. A., eds. Development, function and evolution of teeth. Academic Press, London.Google Scholar
Tyndale-Biscoe, H., and Renfree, M. B. 1987. Reproductive physiology of marsupials. Cambridge University Press, Cambridge.Google Scholar
Ungar, P. S. 2010. Mammal teeth. Johns Hopkins University Press, Baltimore.CrossRefGoogle Scholar
van Nievelt, A. F. H., and Smith, K. K. 2005a. To replace or not to replace: the significance of reduced functional tooth replacement in marsupial and placental mammals. Paleobiology 31:324–346.Google Scholar
van Nievelt, A. F. H., 2005b. Tooth eruption in Monodelphis domestica and its significance for phylogeny and natural history. Journal of Mammalogy 86:333–341.Google Scholar
Voss, R. S., and Jansa, S. A. 2003. Phylogenetic studies on didelphid marsupials II. Non molecular data and new IRBP sequences: separate and combined analyses of didelphine relationships with denser taxon sampling. Bulletin of the American Museum of Natural History 276:1–82.Google Scholar
Voss, R. S., Lunde, D. P., and Simmons, N. B. 2001. The mammals of Paracou, French Guiana: a neotropical lowland rainforest fauna, Part 2. Nonvolant species. Bulletin of the American Museum of Natural History 263:1–236.Google Scholar
Werdelin, L. 1986. Comparison of skull shape in marsupial and placental carnivores. Australian Journal of Zoology 34:109–117.Google Scholar
Werdelin, L. 1987. Jaw geometry and molar morphology in marsupial carnivores: analysis of a constraint and its macroevolutionary consequences. Paleobiology 13:342–350.Google Scholar
Werdelin, L. 1988. Circumventing a constraint: the case of Thylacoleo (Marsupialia, Thylacoleonidae). Australian Journal of Zoology 36:565–571.Google Scholar
Winge, H. 1882. Om Pattedyrenes Tandskifte, isaer med Hensyn til Taendernes Former. Videnskabelige Meddelelser Dansk Naturhistorisk Forening Copenhagen, series 4, 4:15–67.Google Scholar
Wroe, S., and Archer, M. 1995. Extraordinary diphyodonty-related change in dental function for a tooth of the extinct marsupial Ekaltadeta ima (Propleopinae, Hypsiprymnodontidae). Archives of Oral Biology 40:597–603.Google Scholar
Wroe, S., and Milne, N. 2007. Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evolution 61:1251–1260.Google Scholar
Wroe, S., Myers, T. J., Wells, R. T., and Gillespie, A. 1999. Estimating the weight of the Pleistocene marsupial lion, Thylacoleo carnifex (Thylacoleonidae: Marsupialia): implications for the ecomorphology of a marsupial super-predator and hypotheses of impoverishment of Australian marsupial carnivore faunas Australian Journal of Zoology 47:489–498.Google Scholar
Wroe, S., Argot, C., and Dickman, C. 2004. On the rarity of big fierce carnivores and primacy of isolation and area: tracking large mammalian carnivore diversity on two isolated continents. Proceedings of the Royal Society of London B 271:1203–1211.Google Scholar
Zack, S. P. 2012. Deciduous dentition of Didymictis (Carnivoramorpha: Viverravidae): implications for the first appearance of “Creodonta.” Journal of Mammalogy 93:808–817.Google Scholar