Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-26T08:59:49.574Z Has data issue: false hasContentIssue false
  • English
  • Français

Variability, selection, and constraints: development and evolution in viverravid (Carnivora, Mammalia) molar morphology

Published online by Cambridge University Press:  08 February 2016

P. David Polly
P. David Polly*
Affiliation:
Department of Anatomy, Queen Mary and Westfield College, London E1 4NS, United Kingdom Department of Palaeontology, The Natural History Museum, London. E-mail: d.polly@qmw.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Developmental constraints presumably operate by influencing patterns of variability: when development causes some features to vary more than others and when the level of variability is correlated with evolutionary change, then development can be said to constrain evolution. This idea was tested by examining the relationship between tooth variation and three other factors: developmental processes, tooth function, and evolutionary change. Data came from two lineages of viverravid carnivorans (Viverravidae, Carnivora) from the Paleogene of North America. Variability in cusp position was significantly correlated with position in the developmental cascade, with the amount of intercusp growth (when growth is relatively greater in some cusps than others), and with amount of evolutionary change. This indicates that tooth development exerts a local constraint on phenotypic variability and on the evolutionary response to functional selection, but comparative data suggest that the developmental constraint itself may evolve. Intense directional or stabilizing selection may modify the developmental cascade so that the constraint is either removed or modified to permit new evolutionary patterns. Thus development does not constrain evolution in an absolute sense, but rather introduces modifiable patterns of covariance among crown features. Both development and function seem to play important, intertwined roles in coordinating evolutionary change in mammalian molars.

Type
Articles
Information
Paleobiology , Volume 24 , Issue 4 , Fall 1998 , pp. 409 - 429
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

Alberch, P. 1980. Ontogenesis and morphological diversification. American Zoologist 20:653–667.CrossRefGoogle Scholar
Archer, M. 1974. The development of premolar and molar crowns of Antechinus flavipes (Marsupialia, Dasyuridae) and the significance of cusp ontogeny in mammalian teeth. Journal of the Royal Society of Western Australia 57:118–125.Google Scholar
Atchley, W. R., and Hall, B. K. 1991. A model for development and evolution of complex structures. Biological Reviews 66:101–157.CrossRefGoogle Scholar
Barton, N., and Turelli, M. 1989. Evolutionary quantitative genetics: how little do we know? Annual Review of Genetics 23:337–370.CrossRefGoogle ScholarPubMed
Bodenbender, B. E. 1995. Morphological, crystallographic, and stratigraphic data in cladistic analyses of blastoid phylogeny. Contributions from the Museum of Paleontology, University of Michigan 29:201–257.Google Scholar
Bookstein, F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge.Google Scholar
Bookstein, F. L. 1996. Combining the tools of geometric morphometrics. Pp. 131–151in Marcus, L. F., Corti, M., Loy, A., Naylor, G. J., and Slice, D. E., eds. Advances in morphometrics. Plenum, New York.CrossRefGoogle Scholar
Butler, P. M. 1956. The ontogeny of molar pattern. Biological Reviews 31:30–70.CrossRefGoogle Scholar
Butler, P. M. 1967a. The prenatal growth of the human first upper permanent molar. Archives of Oral Biology 12:551–563.CrossRefGoogle ScholarPubMed
Butler, P. M. 1967b. Relative growth within the human first upper permanent molar during the prenatal period. Archives of Oral Biology 12:983–992.CrossRefGoogle ScholarPubMed
Caldwell, M. W. 1994. Developmental constraints and limb evolution in Permian and extant lepidosauromorph diapsids. Journal of Vertebrate Paleontology 14:459–471.CrossRefGoogle Scholar
Charlesworth, B., Lande, R., and Slatkin, M. 1982. A neo-Darwinian commentary on macroevolution. Evolution 36:474–498.Google ScholarPubMed
Cheverud, J. M. 1984. Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology 110:155–171.CrossRefGoogle ScholarPubMed
Cheverud, J. M., Rutledge, J. J., and Atchley, W. R. 1983. Quantitative genetics of development: genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution 37:895–905.Google ScholarPubMed
Clyde, W. C., and Fisher, D. C. 1997. Comparing the fit of stratigraphic and morphologic data in phylogenetic analysis. Paleobiology 23:1–19.CrossRefGoogle Scholar
Crompton, A. W. 1971. The origin of the tribosphenic molar. Pp. 65–87in Kermack, D. A. and Kermack, K. A., eds. Early mammals. Academic Press, London.Google Scholar
Crompton, A. W., and Hiiemae, K. 1970. Molar occlusion and mandibular movements during occlusion in American opossum, Didelphis marsupialis. Zoological Journal of the Linnaean Society 49:21–47.CrossRefGoogle Scholar
Fisher, D. C. 1991. Phylogenetic analysis and its application in evolutionary paleobiology. In Galinsky, N. L. and Signor, P. W., eds. Analytical paleobiology. Short Courses in Paleontology 4:103–122. Paleontological Society, Knoxville, Tenn.Google Scholar
Fisher, D. C. 1992. Stratigraphic parsimony. Pp. 124–129in Maddison, W. P. and Maddison, D. R., eds. MacClade: analysis of phylogeny and character evolution, Version 3. Sinauer Associates, Sunderland, Mass.Google Scholar
Fisher, D. C. 1994. Stratocladistics: morphological and temporal patterns and their relation to phylogenetic process. Pp. 133–171in Grande, L. and Rieppel, O., eds. Interpreting the hierarchy of nature. Academic Press, New York.Google Scholar
Foote, M., and Cowie, R. H. 1988. Developmental buffering as a mechanism for stasis: evidence from the pulmonate Theba pisana. Evolution 42:396–398.Google ScholarPubMed
Fortelius, M. 1985. Ungulate cheek teeth: development, functional, and evolutionary interactions. Acta Zoologica Fennica 180:1–76.Google Scholar
Gingerich, P. D. 1993. Quantification and comparison of evolutionary rates. American Journal of Science 293A:453–478.CrossRefGoogle Scholar
Goodall, C. R. 1991. Procrustes methods in the statistical analysis of shape (with discussion and rejoinder). Journal of the Royal Statistical Society B 52:285–339.Google Scholar
Hall, B. K., and Hörstadius, S. 1988. The neural crest. Oxford University Press, London.Google Scholar
Hershkovitz, P. 1971. Basic crown patterns and cusp homologies in mammalian teeth. Pp. 95–150in Dahlberg, A. A., ed. Dental morphology and evolution. University of Chicago Press, Chicago.Google Scholar
Holder, N. 1983. Developmental constraints and the evolution of vertebrate limb patterns. Journal of Theoretical Biology 104:451–471.CrossRefGoogle Scholar
Hotelling, H. 1931. The generalization of Student's ratio. Annals of Mathematical Statistics 2:360–378.CrossRefGoogle Scholar
Hunter, J. P., and Jernvall, J. 1995. The hypocone as a key innovation in mammalian evolution. Proceedings of the National Academy of Sciences USA 92:10718–10722.CrossRefGoogle ScholarPubMed
Jernvall, J. 1995. Mammalian molar cusp patterns: developmental mechanisms of diversity. Acta Zoologica Fennica 198:1–61.Google Scholar
Jernvall, J. 1997. Developmental basis of mammalian molar cusp evolution. Journal of Vertebrate Paleontology 17(Suppl.):56A.Google Scholar
Jernvall, J., Kettunen, P., Karavanova, I., Martin, L. B., and Thesleff, I. 1994. Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: non-dividing cells express growth stimulating Fgf-4 gene. International Journal of Developmental Biology 38:463–469.Google ScholarPubMed
Jernvall, J., Åberg, T., Kettunen, P., Keränen, S., and Thesleff, I. 1998. The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development 125:161–169.CrossRefGoogle ScholarPubMed
Kauffman, S. A. 1993. The origins of order: self-organization and selection in evolution. Oxford University Press, Oxford.CrossRefGoogle Scholar
Kay, R. F., and Hiiemae, K. M. 1974. Jaw movement and tooth use in recent and fossil primates. American Journal of Physical Anthropology 40:227–256.CrossRefGoogle ScholarPubMed
Kirkpatrick, M., and Lofsvold, D. 1992. Measuring selection and constraint in the evolution of growth. Evolution 46:954–971.CrossRefGoogle ScholarPubMed
Klingenberg, C. P. 1996. Multivariate allometry. Pp. 23–49in Marcus, L. F., Corti, M., Loy, A., Naylor, G. J., and Slice, D. E., eds. Advances in morphometrics. Plenum, New York.CrossRefGoogle Scholar
Kollar, E. J., and Lumsden, A. G. S. 1979. Tooth morphogenesis: the role of the innervation during induction and pattern formation. Journal Biologie Buccale 7:49–60.Google ScholarPubMed
Levene, H. 1960. Robust tests for equality of variances. Pp. 278–292in Olkin, I., Ghurye, S. G., Hoefding, W., Madow, W. G., and Mann, H. B., eds. Contributions to probability and statistics. Stanford University Press, Stanford, Calif.Google Scholar
Lumsden, A. G. S. 1987. The neural crest contribution to tooth development in the mammalian embryo. Pp. 261–300in Maderson, P. F. A., ed. Developmental and evolutionary aspects of the neural crest. Wiley, New York.Google Scholar
Lumsden, A. G. S. 1988. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103(Suppl.):155–170.CrossRefGoogle ScholarPubMed
MacLeod, N.In press. Generalizing and extending the eigen-shape method of shape visualization and analysis. Paleobiology.Google Scholar
Marshall, P. M., and Butler, P. M. 1966. Molar cusp development in the bat, Hipposideros beatus, with reference to the ontogenetic basis of occlusion. Archives of Oral Biology 11:949–965.CrossRefGoogle Scholar
Maynard Smith, J. 1983. The genetics of stasis and punctuation. Annual Review of Genetics 17:11–25.CrossRefGoogle Scholar
Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., and Wolpert, L. 1985. Developmental constraints and evolution. Quarterly Review of Biology 60:265–287.CrossRefGoogle Scholar
Müller, G. B., and Alberch, P. 1990. Ontogeny of the limb skeleton in Alligator mississippiensis: development invariance and change in the evolution of archosaur limbs. Journal of Morphology 203:151–164.CrossRefGoogle ScholarPubMed
Oster, G., Shubin, N., Murray, J., and Alberch, P. 1988. Evolution and morphogenetic rules: the shape of the vertebrate limb in ontogeny and phylogeny. Evolution 42:862–884.CrossRefGoogle ScholarPubMed
Polly, P. D. 1993. Default developmental pathways and functional constraints in the evolution of mammalian molars. Journal of Vertebrate Paleontology 13(Suppl.):53A.Google Scholar
Polly, P. D. 1997. Ancestry and species definitions: a stratocladistic analysis of Viverravidae (Carnivora, Mammalia) from Wyoming. In Contributions from the Museum of Paleontology, University of Michigan 30:1–53. Ann Arbor.Google Scholar
Raff, R. A. 1996. The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Rieppel, O. 1992. Studies on skeleton formation in reptiles. III. Patterns of ossification in the skeleton of Lacerta vivipara Jacquin (Reptilia, Squamata). Fieldiana (Zoology) new series 68:1–25.Google Scholar
Robertson, A. 1956. The effect of selection against extreme deviants based on deviation or on homozygosis. Journal of Genetics 54:236–248.CrossRefGoogle Scholar
Rohlf, F. J., and Slice, D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39:40–59.CrossRefGoogle Scholar
Ruch, J. V. 1990. Patterned distribution of differentiating dental cells: facts and hypotheses. Journal Biologie Buccale 18:91–98.Google ScholarPubMed
Schmalhausen, I. I. 1946. Faktory evolyutsii. Teoria stabiliziruyushchego otbora (Factors of evolution: the theory of stabilizing selection). Academy of Sciences USSR, Moscow. Translated by I. Dordick 1986. University of Chicago Press, Chicago.Google Scholar
Shubin, N., and Alberch, P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evolutionary Biology 20:319–187.Google Scholar
Sober, E. 1984. The nature of selection. University of Chicago Press, Chicago.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Thesleff, I., and Sahlberg, C. 1996. Growth factors as inductive signals regulating tooth morphogenesis. Seminars in Cell and Developmental Biology 7:185–193.CrossRefGoogle Scholar
Van Valen, L. 1978. The statistics of variation. Evolutionary Theory 4:33–43.Google Scholar
Viriot, L., Peterkova, R., Vonesch, J. L., Peterka, M., Ruch, J. V., and Lesot, H. 1997. Mouse molar morphogenesis revisited by three-dimensional reconstruction. 3. Spatial distribution of mitoses and apoptoses up to bell-staged first lower molar teeth. International Journal of Developmental Biology 41:679–690.Google Scholar
Waddington, C. H. 1942. The canalisation of development and the inheritance of acquired characters. Nature 150:563.CrossRefGoogle Scholar
Waddington, C. H. 1956. Genetic assimilation of the bithorax phenotype. Evolution 10:1–13.CrossRefGoogle Scholar
Waddington, C. H. 1957a. The strategy of the genes. George Allen Unwin, London.Google Scholar
Waddington, C. H. 1957b. The genetic basis of the assimilated bithorax stock. Journal of Genetics 55:240–245.CrossRefGoogle Scholar
Wake, D. B., and Larson, A. 1987. A multidimensional analysis of an evolving lineage. Science 238:42–48.CrossRefGoogle ScholarPubMed
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Wright, S. 1968. Evolution and the genetics of populations, Vol. 1. Genetic and biometric foundations. University of Chicago Press, Chicago.Google Scholar
Zelditch, M. L., Bookstein, F. L., and Lundgrian, B. L. 1992. Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46:1164–1180.CrossRefGoogle ScholarPubMed
Zelditch, M. L. 1993. The ontogenetic complexity of developmental constraints. Journal of Evolutionary Biology 6:621–641.CrossRefGoogle Scholar