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Variation and covariation of skulls and teeth: modern carnivores and the interpretation of fossil mammals

Published online by Cambridge University Press:  08 April 2016

Tamar Dayan
Affiliation:
Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel E-mail: dayant@post.tau.ac.il
David Wool
Affiliation:
Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel E-mail: dayant@post.tau.ac.il
Daniel Simberloff
Affiliation:
Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996-1610

Abstract

Teeth are generally the best-preserved elements among mammal fossil remains and are highly diagnostic characters. Consequently, much mammalian paleontological, systematic, and evolutionary research focuses on teeth, so it is important to understand how they vary and covary with other characters. Dental traits within populations of carnivores appear to be more variable than cranial traits, a pattern that results only partly from their usually smaller size. Furthermore, dental traits, although highly correlated with one another, are not highly correlated with cranial traits, which are also highly correlated with one another. Thus, teeth and cranial bones may be subject to quite different selective pressures and genetic/developmental constraints and may suggest different microevolutionary scenarios. Vestigial teeth show significantly greater variability than expected, reflecting the absence of stabilizing selection.

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Articles
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Copyright © The Paleontological Society 

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References

Literature Cited

Alpatov, W. W., and Boschko-Stepanenko, A. M. 1928. Variation and correlation in serially situated organs in insects, fishes and birds. American Naturalist 62:409424.Google Scholar
Atchley, W. R. 1987. Developmental quantitative genetics and the evolution of ontogenies. Evolution 41:316330.Google Scholar
Atchley, W. R., Plummer, A. A., and Riska, B. 1985a. Genetics of mandibular size and shape in the mouse. Genetics 111:555557CrossRefGoogle ScholarPubMed
Atchley, W. R., Plummer, A. A., and Riska, B. 1985b. A genetic analysis of size scaling in the mouse mandible. Genetics 111:579595.Google Scholar
Bader, R. S., and Hall, J. S. 1960. Osteometric variation and function in bats. Evolution 14:817.Google Scholar
Badyaev, A. V. 1998. Environmental stress and developmental stability in dentition of the Yellowstone grizzly bears. Behavioral Ecology 9:339344.CrossRefGoogle Scholar
Bateson, W. 1894. Materials for the study of variation. Macmillan, London.Google Scholar
Bermudez-De Castro, J. M. 1993. The Atapuerca dental remains: new evidence (1987–1991 excavations) and interpretations. Journal of Human Evolution 24:339371.Google Scholar
Bookstein, F. L. 1989. “Size and shape”: a comment on semantics. Systematic Zoology 38:173180.Google Scholar
Bronner, G. N. 1996. Non-geographic variation in morphological characteristics of the Hottentot golden mole, Amblysomus hottentotus (Insectivora: Chrysochloridae). Mammalia 60:702727.Google Scholar
Butler, P. M. 1939. Studies of the mammalian dentition: differentiation of the post-canine dentition. Proceeedings of the Zoological Society of London B 109:136.Google Scholar
Carrasco, M. A. 1998. Variation and its implications in a population of Cupidinimus (Heteromyidae) from Hepburn's Mesa, Montana. Journal of Vertebrate Paleontology 18:391402.Google Scholar
Chaline, J., and Laurin, B. 1986. Phyletic gradualism in a European Plio-Pleistocene Mimomys lineage (Arvicolidae, Rodentia). Paleobiology 12:203216.CrossRefGoogle Scholar
Cheverud, J. M. 1982. Phenotypic, genetic and environmental morphological integration in the cranium. Evolution 36:499516.Google Scholar
Cheverud, J. M. 1989. A comparative analysis of morphological variation patterns in the papionins. Evolution 43:17371747.Google Scholar
Cheverud, J. M. 1995. Morphological integration in the saddle-back tamarin (Sanguinus fuscicollis) cranium. American Naturalist 145:6389.Google Scholar
Cheverud, J. M. 1996. Developmental integration and the evolution of pleiotropy. American Zoologist 36:4450.Google Scholar
Cheverud, J. M., Routman, E. J., and Irschick, D. J. 1997. Pleiotropic effects of individual gene loci on mandibular morphology. Evolution 51:20062016.Google Scholar
Cope, D. A. 1993. Measures of dental variation as indicators of multiple taxa in samples of sympatric Cercopithecus species. Pp. 211237in Kimbel, W. H. and Martin, L. B., eds. Species, species concepts, and primate evolution. Plenum, New York.Google Scholar
Cope, D. A., and Lacy, M. G. 1995. Comparative application of the coefficient of variation and range-based statistics for assessing the taxonomic composition of fossil samples. Journal of Human Evolution 29:549576.Google Scholar
Creighton, G. K. 1980. Static allometry of mammalian teeth and the correlation of tooth size and body size in contemporary mammals. Journal of Zoology 191:435443.Google Scholar
Damuth, J., and MacFadden, B. J. 1990. Introduction: body size and its estimation. Pp. 110in Damuth, and MacFadden, 1990.Google Scholar
Damuth, J., and MacFadden, B. J., eds. 1990. Body size in mammalian paleobiology. Cambridge University Press, Cambridge.Google Scholar
Dayan, T., and Simberloff, D. 1994a. Morphological relationships among co-existing heteromyids: an incisive dental character. American Naturalist 143:462477.CrossRefGoogle Scholar
Dayan, T., and Simberloff, D. 1994b. Character displacement, sexual size dimorphism, and morphological variation among the mustelids of the British Isles. Ecology 75:10631073.Google Scholar
Dayan, T., and Simberloff, D. 1998. Size patterns among competitors: ecological character displacement and character release in mammals, with special references to island populations. Mammal Review 28:99124.Google Scholar
Dayan, T., Simberloff, D., Tchernov, E., and Yom-Tov, Y. 1989a. Inter- and intraspecific character displacement in mustelids. Ecology 70:15261539.Google Scholar
Dayan, T., Simberloff, D., Tchernov, E., and Yom-Tov, Y. 1989b. Ecological character displacement in Saharo-Arabian Vulpes: outfoxing Bergmann's rule. Oikos 55:263272.Google Scholar
Dayan, T., Simberloff, D., Tchernov, E., and Yom-Tov, Y. 1990. Feline canines: community-wide character displacement in the small cats of Israel. American Naturalist 136:3960.Google Scholar
Dayan, T., Simberloff, D., Tchernov, E., and Yom-Tov, Y. 1992. Canine carnassials: community-wide character displacement among the wolves, jackals, and foxes of Israel. Biological Journal of the Linnean Society 45:315331.Google Scholar
Driesch, A. von den. 1976. A guide to the measurement of animal bones from archaeological sites. Peabody Museum Bulletin 1:1137. Harvard University, Cambridge.Google Scholar
Fleagle, J. G. 1989. Sexual dimorphism in Laccopithecus robustus, a Late Miocene hominoid from China. American Journal of Physical Anthropology 79:137.Google Scholar
Fortelius, M. 1990. Problems in estimating body sizes of extinct mammals. Pp. 207228in Damuth, and MacFadden, 1990.Google Scholar
Garn, S. M., and Lewis, A. B. 1958. Tooth-size, body-size and “giant” fossil man. American Anthropologist 60:874880.Google Scholar
Garn, S. M., Osbortne, R. H., and McCabe, K. D. 1979. The effect of prenatal factors on crown dimensions. American Journal of Physical Anthropology 51:665678.Google Scholar
Gingerich, P. D. 1974. Size variability of the teeth in living mammals and the diagnosis of closely related sympatric fossil species. Journal of Paleontology 48:895903.Google Scholar
Gingerich, P. D. 1981. Variation, sexual dimorphism, and social structure in the early Eocene horse Hyracotherium (Mammalia, Perissodactyla). Paleobiology 7:443455.Google Scholar
Gingerich, P. D. 1985. Species in the fossil record: concepts, trends and transition. Paleobiology 11:2741.Google Scholar
Gingerich, P. D., and Schoeninger, M. J. 1979. Patterns of tooth size variability in the dentition of primates. American Journal of Physical Anthropology 51:457466.Google Scholar
Gingerich, P. D., and Winkler, D. A. 1979. Patterns of variation and correlation in the dentition of the red fox, Vulpes vulpes. Journal of Mammalogy 60:691704.CrossRefGoogle Scholar
Gingerich, P. D., Smith, B. H., and Rosenberg, K. 1982. Allometric scaling in the dentition of primates and predictions of body weight in fossils. American Journal of Physical Anthropology 58:81100.Google Scholar
Glass, G. E., and Todd, N. B. 1977. Quasi-continuous variation of the second upper premolar in Veils bengalensis Kerr, 1792 and its significance for some fossil lynxes. Zeitschrift für Saugetierkünde 42:3644.Google Scholar
Gould, S. J. 1975. On the scaling of tooth size in mammals. American Zoologist 15:315362.Google Scholar
Gould, S. J., and Garwood, R. A. 1969. Levels of integration in mammalian dentitions: an analysis of correlations in Nesophontes micrus (Insectivora) and Oryzomys couesi (Rodentia). Evolution 23:276300.Google Scholar
Harris, E. F., and Rathbun, T. A. 1989. Small tooth sizes in a nineteenth century South Carolina plantation slave series. American Journal of Physical Anthropology 78:411420.Google Scholar
Harrison, D. L. 1968. The mammals of Arabia. Ernest Benn, London.Google Scholar
Henderson, A. M., and Corruccini, R. S. 1976. Relationship between tooth size and body size in American blacks. Journal of Dental Research 55:9496.Google Scholar
Hilborn, R., and Mangel, M. 1997. The ecological detective: confronting models with data. Princeton University Press, Princeton, N.J.Google Scholar
Hillson, S. 1996. Dental anthropology. Cambridge University Press, Cambridge.Google Scholar
Hoffmann, A. A., and Merila, J. 1999. Heritable variation and evolution under favorable and unfavorable conditions. Trends in Ecology and Evolution 14:96101.Google Scholar
Holmes, T. 1987. Sexual dimorphism in North American weasels with a phylogeny of Mustelidae. Ph.D. dissertation. University of Kansas, Lawrence.Google Scholar
Hunter, J. P., and Fortelius, M. 1994. Comparative dental occlusal morphology, facet development, and microwear in two sympatric species of Listriodon (Mammalia, Suidae) from the Middle Miocene of western Anatolia (Turkey). Journal of Vertebrate Paleontology 14:105126.Google Scholar
Hussain, S. T. 1971. Revision of Hipparion (Equidae: Mammalia) from the Siwalik Hills of Pakistan and India. Bayerische Akademie der Wissenschaften, Abhandlungen 147:168.Google Scholar
Janis, C. M. 1990. Correlation of dental and cranial variables with body size in ungulates and macropodoids. Pp. 255299in Damuth, and MacFadden, 1990.Google Scholar
Jernvall, J. 2000. Linking development with generation of novelty in mammalian teeth. Proceedings of the National Academy USA 97:26312645.Google Scholar
Jernvall, J., and Thesleff, I. 2000. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mechanisms of Development 92:1929.Google Scholar
Jervnvall, J., Hunter, J. P., and Fortelius, M. 1996. Molar tooth diversity, disparity, and ecology in Cenozoic ungulate radiations. Science 274:14891492.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
Jolicoeur, P., and Mosimann, J. E. 1960. Size and shape variation in the painted turtle: a principal components analysis. Growth 24:339354.Google Scholar
Kay, R. F. 1975. Allometry and early hominids. Science 189:63.Google Scholar
Keeping, E. S. 1962. Introduction to statistical inference. Van Nostrand, Princeton, N.J.Google Scholar
Kerfoot, W. C. 1988. Defensive spines: inverse relationship between coefficients of variation and size. Limnology and Oceanography 33:14121429.Google Scholar
Kieser, J. A. 1990. Human adult odontometrics. Cambridge Studies in Biological Anthropology 4. Cambridge University Press, Cambridge.Google Scholar
Kieser, J. A., and Groenveld, H. T. 1988. Allometric relations of teeth and jaws in man. American Journal of Physical Anthropology 77:5768.Google Scholar
Kieser, J. A., and Groenveld, H. T. 1990. Static intraspecific allometry of the dentition in Otolemur crassicaudatus. Zoological Journal of the Linnean Society 98:295306.Google Scholar
Klevezal, G. A., and Sokolov, A. A. 1999. Retrospectively evaluating the condition of a reindeer population that inhabited the Novaya Zemlya Archipelago during nuclear tests. Zoologichesky Zhurnal 78:102111.Google Scholar
Koch, P. L. 1986. Clinal geographic variation in mammals: implications for the study of chronoclines. Paleobiology 12:269281.Google Scholar
Kurtén, B. 1953. On the variation and population dynamics of fossil and recent mammal populations. Acta Zoologica Fennica 76:1122.Google Scholar
Kurtén, B. 1954. Observations on the allometry in mammalian dentitions: its interpretation and evolutionary significance. Acta Zoologica Fennica 85:113.Google Scholar
Kurtén, B. 1967. Some quantitative approaches to dental microevolution. Journal of Dental Research 46:817828.Google Scholar
Lande, R. 1977. On comparing coefficients of variation. Systematic Zoology 26:214217.Google Scholar
Lavelle, C. L. B. 1974. Relationship between tooth size and skull size. Journal of Dental Research 53:1301.Google Scholar
Legendre, S. 1982. Hipposideridae (Mammalia: Chiroptera) from the Mediterranean Middle and Late Neogene, and evolution of the genera Hipposideros and Asellia. Journal of Vertebrate Paleontology 2:372385.Google Scholar
Legendre, S., and Roth, C. 1988. Correlation of carnassial tooth size and body weight in recent carnivores (Mammalia). Historical Biology 1:8598.Google Scholar
Leutenegger, W., and Shell, B. 1987. Variability and sexual dimorphism in canine size of Australopithecus and extant hominoids. Journal of Human Evolution 16:359367.Google Scholar
Lombardi, A. V. 1975. A factor analysis of morphogenetic fields in the human dentition. American Journal of Physical Anthropology 42:99104.Google Scholar
MacFadden, B. J. 1986. Fossil horses from “Eohippus” (Hyracotherium) to Equus: scaling Cope's Law and the evolution of body size. Palaeontology 12:355369.Google Scholar
Marshall, L. G., and Corruccini, R. S. 1978. Variability, evolutionary rates, and allometry in dwarfing lineages. Paleobiology 4:101119.CrossRefGoogle Scholar
McKinney, M. L. 1990. Trends in body-size evolution. Pp. 75118in McNamara, K., ed. Evolutionary trends. University of Arizona Press, Tucson.Google Scholar
Mezzabotta, C., Masini, F., and Torre, D. 1995. Microtus (Tyrrhenicola) henseli, endemic fossil vole from Pleistocene and Holocene localities of Sardinia and Corsica: Evolutionary patterns and biochronological meansing. Bollettino della Societa Paleontologica Italiana 34:81104.Google Scholar
Neff, N. A., and Marcus, L. F. 1980. A survey of multivariate methods for systematics. Privately published, New York.Google Scholar
Osborn, J. W. 1978. Morphogenetic gradients: fields vs. clones. Pp. 171201in Butler, P. M. and Joysey, K. A., eds. Development, function and evolution of teeth. Academic Press, London.Google Scholar
Pankakoski, E., Vaisanen, R. A., and Nurmi, K. 1987. Variability of muskrat skulls: measurement error, environmental modification and size allometry. Systematic Zoology 36:3551.Google Scholar
Pearson, K., and Davin, A. G. 1924. On the biometric constants of the human skull. Biometrica 16:328363.Google Scholar
Pengilly, D. 1984. Developmental vs. functional explanations for the patterns of variability and correlation in the dentition of foxes. Journal of Mammalogy 63:3443.Google Scholar
Polly, P. D. 1998a. Variability in mammalian dentitions: size-related bias in the coefficient of variation. Biological Journal of the Linnean Society 64:8399.Google Scholar
Polly, P. D. 1998b. Variability, selection, and constraints: development and evolution in viverravid (Carnivora, mammalia) molar morphology. Paleobiology 24:409429.Google Scholar
Prothero, D. R., and Sereno, P. C. 1982. Allometry and paleoecology of middle Miocene dwarf rhinoceroses from the Texas Gulf coastal plain. Paleobiology 8:1630.Google Scholar
Radinsky, L. B. 1981. Evolution of skull shape in carnivores. I. Representative modern carnivores. Biological Journal of the Linnean Society 15:369388.Google Scholar
Rohlf, F. J. 1986. NTSYS-PC, numerical taxonomy and multivariate analysis system, Version 1.50. Exeter Software, Setauket, N.Y.Google Scholar
Rohlf, F. J., Gilmartin, A. J., and Hart, G. 1983. The Kluge-Kerfoot phenomenon—a statistical artifact. Evolution 37:180202.Google Scholar
Romer, A. S. 1953. Vertebrate paleontology, 2d ed.University of Chicago Press, Chicago.Google Scholar
Roth, V. L. 1990. Insular dwarf elephants: a case study in body mass estimation and ecological inference. Pp. 151179in Damuth, and MacFadden, 1990.Google Scholar
Roth, V. L. 1992. Quantitative variation in elephant dentitions: implications for the delimitation of fossil species. Paleobiology 18:184202.Google Scholar
Roth, V. L. 1996. Cranial integration in the Sciuridae. American Zoologist 36:1423.Google Scholar
Schoch, R. M., and Lucas, S. G. 1981. The systematics of stylinodon, an Eocene taeniodont (Mammalia) from western North America. Journal of Vertebrate Paleontology 1:175183.Google Scholar
Searle, A. G. 1959. The study of variation in Singapore cats. Journal of Genetics 56:116.Google Scholar
Shea, B. T., and Gomez, A. M. 1988. Tooth scaling and evolutionary dwarfism: an investigation of allometry in human pygmies. American Journal of Physical Anthropology 77:117132.Google Scholar
Simpson, G. C., Roe, A., and Lewontin, R. C. 1960. Quantitative zoology. Harcourt, Brace, New York.Google Scholar
Smith, K. K. 1996. Integration of craniofacial structures during development in mammals. American Zoologist 36:7079.Google Scholar
Smith, M. F., and Patton, J. L. 1988. Subspecies of pocket gophers: causal bases for geographic differentiation in Thomomys bottae. Systematic Zoology 37:163178.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1981. Biometry: the principles and practices of statistics in biological research. W. H. Freeman, New York.Google Scholar
Soulé, M. 1982. Allomeric variation. I. The theory and some consequences. American Naturalist 120:751764.Google Scholar
Suchentrunk, F., and Flux, J. E. C. 1996. Minor dental traits in East African cape hares and savanna hares (Lepus capensis and Lepus victoriae): a study of intra- and interspecific variability. Journal of Zoology 238:495511.Google Scholar
Tague, R. G. 1997. Variability of a vestigial structure: fist metacarpal in Colobus guereza and Ateles geoffroyi. Evolution 51:595605.Google Scholar
Thackeray, J. F. 1997. Morphometric, palaeoecologial and taxonomic considerations of southern African zebras: attempts to distinguish the quagga. South African Journal of Science 93:8993.Google Scholar
Todd, N. B., Glass, G. E., and McClure, I. 1974. Gene frequencies in some cats in South America: Caracas, Venezuela; Willemstad, Curacao. Carnivore Genetics Newsletter 2:23235.Google Scholar
Tsoukala, E. 1996. Comparative study of ursid remains from the Quaternary of Greece, Turkey and Israel. Acta Zoologica Cracoviensia 39:571576.Google Scholar
Van Valkenburgh, B. 1988. Trophic diversity in past and present guilds of large predatory mammals. Paleobiology 14:155173.Google Scholar
Van Valkenburgh, B., and Wayne, R. 1994. Shape divergence associated with size convergence in sympatric East African jackals. Ecology 75:15671581.Google Scholar
Voss, R. T. 1988. Systematics and ecology of Ichthyomine rodents (Muroidea): patterns of morphological evolution in a small adaptive radiation. Bulletin of the American Museum of Natural History 188:259493.Google Scholar
West, R. M. 1979. Apparent prolonged evolutionary stasis in the middle Eocene hoofed mammal Hypsodus. Paleobiology 5:252260.Google Scholar
Wolpoff, M. H. 1985. Tooth size-body scaling in a human population: theory and practice of an allometric analysis. Pp. 273318in Jungers, W. L., ed. Size and scaling in primate biology. Plenum, New York.Google Scholar
Yablokov, A. V. 1974. Variability in mammals. Amerind, New Delhi.Google Scholar
Zelditch, M. L. 1988. Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution 42:2841.Google Scholar
Zelditch, M. L. 1996. Introduction to the symposium: historical patterns of development integration. American Zoologist 36:13.Google Scholar