Evolutionary Biology

, Volume 34, Issue 3–4, pp 99–120 | Cite as

Phenotypic Variability: Its Components, Measurement and Underlying Developmental Processes

  • Katherine Elizabeth Willmore
  • Nathan M. Young
  • Joan T. Richtsmeier
Synthesis

Abstract

Variability contrasts with variation in that variability describes the potential for variation, not simply the expressed variation. The power of studying variability lies in creating a conceptual framework around which the relationship between the genotype and phenotype can be understood. Here, we attempt to demonstrate the importance of phenotypic variability, how it structures variation, and how fundamental developmental processes structure variability. Given the broad scope of this topic, we focus on three widely studied properties of variability: canalization, developmental stability and morphological integration. We have organized the paper to emphasize the importance of differentiating between the theory surrounding these components of phenotypic variability, their measurement and the biological factors surrounding their expression. First, we define these properties of variability, how they relate to each other and to variability as a whole. Second, we summarize the common methods of measurement for canalization, developmental stability and morphological integration and the reasoning behind these methods. Finally, we focus on jaw development as an example of how the basic processes of development affect variability and the resultant variation, with emphasis on how processes at all levels of the organismal hierarchy interact with one another and contribute to phenotypic variability.

Keywords

Variability Variation Development Canalization Morphological integration Developmental stability Phenotype 

References

  1. Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101–157.PubMedGoogle Scholar
  2. Babbitt, G. A., Kiltie, R., & Bolker, B. (2006) Are fluctuating asymmetry studies adequately sampled? Implications of a new model for size distribution. American Naturalist, 167, 230–245.Google Scholar
  3. Bagheri, H. C., & Wagner, G. P. (2004). Evolution of dominance in metabolic pathways. Genetics, 168, 1713–1735.PubMedGoogle Scholar
  4. Berg, R. L. (1959). The ecological significance of correlational pleiades. Evolution, 14, 171–180.Google Scholar
  5. Bjorksten, T. A., Fowler, K., & Pomiankowski, A. (2000). What does sexual trait FA tell us about stress? TREE, 15, 163–166.PubMedGoogle Scholar
  6. Blake, W. J., Kaern, M., Cantor, C. R., & Collins, J. J. (2003). Noise in eukaryotic gene expression. Nature, 422, 633–637.PubMedGoogle Scholar
  7. Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics, 13, 115–155.Google Scholar
  8. Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868–873.PubMedGoogle Scholar
  9. Bresin, A., Johansson, C. B., & Kiliaridis, S. (1994). Effects of occlusal strain on the development of the dentoalveolar process in the growing rat. A morphometric study. European Journal of Experimental Musculoskeletal Research, 3, 112–122.Google Scholar
  10. Breuker, C. J., Patterson, J. S., & Klingenberg, C. P. (2006). A single basis for developmental buffering of Drosophila wing shape. PloS ONE 1:e7.Google Scholar
  11. Burnett, R. J., & Larkins, B. A. (1999). Opaque2 modifiers alter transcription of the 27-kDA γ-zein genes in maize. Molecular & General Genetics, 261, 908–916.Google Scholar
  12. Carroll, S. B., Grenier, J. K., & Weatherbee, S. D. (2005). From DNA to diversity: Molecular genetics and the evolution of animal design (2nd ed.). Malden MA: Blackwell Publishing Ltd.Google Scholar
  13. Chernoff, B., & Magwene, P. M. (1999). Morphological integration: Forty years later. In: E. C. Olson, & R. L. Miller (Eds.), Morphological integration (pp. 319–353). Chicago: University of Chicago Press.Google Scholar
  14. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499–516.Google Scholar
  15. Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155–171.PubMedGoogle Scholar
  16. Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42, 958–968.Google Scholar
  17. Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145, 63–89.Google Scholar
  18. Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.Google Scholar
  19. Cheverud, J. M., Routman, E. J., & Irschick, D. J. (1997). Pleiotropic effects of individual gene loci on mandibular morphology. Evolution, 51, 2006–2016.Google Scholar
  20. Cheverud, J. M., Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., & Pletscher, L. S. (2004). Pleiotropic effects on mandibular morphology II: Differential epistasis and genetic variation in morphological integration. Journal of Experimental Zoology (Molecular and Development Evolution), 302B, 424–435.Google Scholar
  21. Ciochon, R. L., Nisbett, R. A., & Corruccini, R. S. (1997). Dietary consistency and craniofacial development related to masticatory function in minipigs. Journal of Craniofacial Genetics and Developmental Biology, 17, 96–102.PubMedGoogle Scholar
  22. Clarke, G. M. (1993). The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica, 89, 15–23.Google Scholar
  23. Clarke, G. M. (1998). The genetic basis of developmental stability, V. Inter- and intra-individual character variation. Heredity, 80, 562–567.Google Scholar
  24. Cole, T. M. III. (2002). MI Boot Windows-based software for bootstrap comparison of morphological integration. University of Missouri–Kansas School of Medicine, Kansas, MO.Google Scholar
  25. Cole, T. M., III, & Lele, S. (2002). Bootstrap-based methods for comparing morphological integration patterns. American Journal of Physical Anthopology, Supplement, 34, 55.Google Scholar
  26. Cottrill, C. P., Archer, C. W., & Wolpert, L. (1987). Cell sorting and chongrogenic aggregate formation in micromass culture. Developmental Biology, 122, 503–515.PubMedGoogle Scholar
  27. Debat, V., Alibert, P., David, P., Paradis, E., & Auffray, J. -C. (2000). Independence between developmental stability and canalization in the skull of the house mouse. Proceedings of Royal Society of London, Series B, 267, 423–430.Google Scholar
  28. Debat, V., Milton, C. C., Rutherford, S., Klingenberg, C. P., & Hoffmann, A. A. (2006). HSP90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution, 60, 2529–2538.PubMedGoogle Scholar
  29. Depew, M. J., Lufkin, T., & Rubenstein, J. L. R. (2002). Specification of jaw subdivisions by Dlx genes. Science, 298, 381–385.PubMedGoogle Scholar
  30. Depew, M. J., Simpson, C. A., Morasso, M., & Rubenstein, J. L. R. (2005). Reassessing the Dlx code: The genetic regulation of branchial arch skeletal pattern and development. Journal of Anatomy, 207, 501–561.PubMedCrossRefGoogle Scholar
  31. Dunn, R. B., & Fraser, A. S. (1958). Selection for an invariant character—“vibrissae number”—in the house mouse. Nature, 181, 1018–1019.Google Scholar
  32. Dunn, R. B., & Fraser, A. S. (1959). Selection for an invariant character, vibrissae number in the house mouse. Australian Journal of Biological Sciences, 12, 506–523.Google Scholar
  33. Eccleston, A, DeWitt, N., Gunter, C., Marte B., & Nath, D. (2007). Epigenetics. Nature, 447, 395.Google Scholar
  34. Ede, D. A. (1983). Cellular condensations and chondrogenesis. In: B. K. Hall (Ed.), Cartilage, development, differentiation and growth, Vol. 2. (pp. 143–186). New York: Academic Press.Google Scholar
  35. Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., Pletscher, L. S., & Cheverud, J. M. (2003). Pleiotropic effects on mandibular morphology I. Developmental morphological integration and differential dominance. Journal of Experimental Zoology (Molecular and Development Evolution), 296B, 58–79.Google Scholar
  36. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. New York: Longman Press.Google Scholar
  37. Fiering, S., Whitelaw, E., & Martin, D. I. K. (2000). To be or not to be active: the stochastic nature of enhancer action. Bioessays, 22, 381–387.PubMedGoogle Scholar
  38. Foote, M., & Cowie, R. H. (1988). Developmental buffering as a mechanism for stasis: Evidence from the pulmonate Theba pisana. Evolution, 42, 396–399.Google Scholar
  39. Francis-West, P. H., Robson, L., & Evans, D. J. R. (2003). Craniofacial development: The tissue and molecular interactions that control development of the head. In: F. Beck, B. Christ, W. Kriz, W. Kummer, E. Marani, R. Putz, Y. Sano, T. H. Schiebler, G. L. Schoenwolf, & K. Zilles (Eds.), Advances in anatomy and cell biology. Vol. 169. Berlin: Springer-Verlag.Google Scholar
  40. Gass, G. L., & Bolker, J. A. (2002). Modularity. In: W. Olson (Ed.), Keywords and concepts in evolutionary developmental biology. Cambridge: Harvard University Press.Google Scholar
  41. Geetha, K. B., Lending, C. R., Lopes, M. A., Wallace, J. C., & Larkins, B. A. (1991). Opaque-2 modifiers increase γ-zein synthesis and alter its spatial distribution in maize endosperm. Plant Cell, 3, 1207–1219.PubMedGoogle Scholar
  42. Gibson, G., & van Helden, S. (1997). Is function of the Drosophila homeotic gene Ultrabithorax canalized? Genetics, 147, 1155–1168.PubMedGoogle Scholar
  43. Gibson, G., & Wagner, G. (2000). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372–380.PubMedGoogle Scholar
  44. Gilbert, S. F. (2003). Developmental biology (7th ed.) Massachusetts: Sinauer Associated Inc.Google Scholar
  45. Gould, S. J., & Garwood, R. A. (1969). Levels of integration in mammalian dentitions: An analysis of correlations in Nesophontes micrus (Insectivora) and Oryzomys couesi (Rodentia). Evolution, 23, 276–300.Google Scholar
  46. Graham, A. (2002). Jaw development: Chinless wonders. Current Biology, 12, 810–812.Google Scholar
  47. Graham, J. H., Freeman, D. C., & Emlen, J. M. (1993). Developmental stability: A sensitive indicator of populations under stress. In: M. A. Lewis (Ed.), Environmental toxicology and risk assessment (pp. 136–158). Philadelphia: American Society for Testing and Materials.Google Scholar
  48. Graham, J. H., Shimizu, K., Emlen, J. M., Freeman, D. C., & Merkel, J. (2003). Growth model and the expected distribution of fluctuating asymmetry. Biological Journal of the Linnean Society, 80, 57–65.Google Scholar
  49. Hall, B. K. (1978). Developmental and cellular skeletal biology. New York: Academic Press.Google Scholar
  50. Hall, B. K. (1988). The embryonic development of bone. American Scientist, 76, 174–181.Google Scholar
  51. Hall, B. K. (1999). The neural crest in development and evolution. New York: Springer-Verlag.Google Scholar
  52. Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology Supplement, 35, 131–158.Google Scholar
  53. He, T., & Kiliaridis, S. (2003). Effects of masticatory muscle function on craniofacial morphology in growing ferrets (Mustela putorius furo). European Journal of Oral Sciences, 111, 510–517.PubMedGoogle Scholar
  54. Hermisson, J., Hansen, T. F., & Wagner, G. P. (2003). Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. American Naturalist, 161, 708–734.PubMedGoogle Scholar
  55. Hermisson, J., & Wagner, G. P. (2004). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372–380.Google Scholar
  56. Herring, S. W. (1993). Epigenetic and functional influences on skull growth. In: J. Hanken, & B. K. Hall (Eds.), The skull, Vol. 1 (pp. 153–206). Chicago: University of Chicago Press.Google Scholar
  57. Herring, S. W., & Teng, S. (2000). Strain in the braincase and its sutures during function. American Journal of Physical Anthropology, 112, 575–593.PubMedGoogle Scholar
  58. Herring, S. W., Decker, J. D., Liu, Z.-J., & Ma, T. (2002). Temporomandibular joint in miniature pigs: anatomy, cell replication, and relation to loading. Anatomical Record, 266, 152–166.PubMedGoogle Scholar
  59. Houle, D. (1998). How should we explain variation in genetic variance of traits? Genetica, 102/103, 241–253.Google Scholar
  60. Huerta-Sanchez, E., & Durrett, R. (2007). Wagner’s canalization model. Theoretical Population Biology, 71, 121–130.PubMedGoogle Scholar
  61. Hurle, J. M., Gana, Y., & Marcias, D. (1989). Experimental analysis of the in-vivo chondrogenic potential of the interdigital mesenchyme of the chick leg bud subjected to local ectodermal removal. Developmental Biology, 132, 368–374.PubMedGoogle Scholar
  62. Jacob, F. (1977). Evolution and tinkering. Science, 196, 1161–1166.PubMedGoogle Scholar
  63. Jernvall, J., & Jung, H. S. (2000). Genotype, phenotype, and developmental biology of molar tooth characters. American Journal of Physical Anthropology, 43, 171–190.Google Scholar
  64. Johnson, D. R. (1986). The genetics of the skeleton. Oxford: Clarendon Press.Google Scholar
  65. Katsaros, C., Berg, R., & Kiliaridis, S. (2002). Influence of masticatory muscle function on transverse skull dimensions in the growing rat. Journal of Orofacial Orthopedics, 63, 5–13.PubMedGoogle Scholar
  66. Kaufmann, W. K., & Paules, R. S. (1996). DNA damage and cell cycle checkpoints. The FASEB Journal, 10, 238–247.PubMedGoogle Scholar
  67. Klingenberg, C. P. (2003). A developmental perspective on developmental instability: Theory, models and mechanisms. In: M. Polak (Ed.), Developmental Instability (DI): Causes and Consequences (pp. 14–34). Oxford: Oxford University Press.Google Scholar
  68. Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric Morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52, 1363–1375.Google Scholar
  69. Klingenberg, C. P., & Zaklan, S. D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54, 1273–1285.PubMedGoogle Scholar
  70. Klingenberg, C. P., Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2001). Genetic architecture of mandible shape in mice: Effects of quantitative trait loci analyzed by geometric morphometrics. Genetics, 157, 785–802.PubMedGoogle Scholar
  71. Kuratani, S. (2005). Developmental studies of the lamprey and hierarchical evolutionary steps towards the acquisition of the jaw. Journal of Anatomy, 207, 489–499.PubMedCrossRefGoogle Scholar
  72. Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2002). An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution, 56, 642–653.PubMedGoogle Scholar
  73. Lens, L., VanDongen, S., Kark, S., & Matthysen, E. (2002). Fluctuating asymmetry as an indicator of fitness: Can we bridge the gap between studies? Biological Reviews, 77, 27–38.PubMedGoogle Scholar
  74. Leung, B., Forbes, M. R., & Houle, D. (2000). Fluctuating asymmetry as an indicator of stress: comparing efficacy of analyses involving multiple traits. American Naturalist, 155, 101–115.PubMedGoogle Scholar
  75. Ludwig, W. (1932). Das Rechts-links problem im Teirreich und beim Menschen. Berlin (Germany): Springer.Google Scholar
  76. Lund, J. P., & Kolta, A. (2006). Generation of the central masticatory pattern and its modification by sensory feedback. Dysphagia, 21, 167–174.PubMedGoogle Scholar
  77. Manning, J. T., & Chamberlain, A. T. (1994). Fluctuating asymmetry in gorilla canines: a sensitive indicator of environmental stress. Proceedings of Royal Society of London, Series B, 255, 189–193.Google Scholar
  78. Marriog, G., & Cheverud, J. M. (2001). A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys. Evolution, 55, 2576–2600.Google Scholar
  79. McAdams, H. H., & Arkin, A. (1999). It’s a noisy business! Genetic regulation at the nanomolar scale. Trends in Genetics, 15, 65–69.Google Scholar
  80. Mills, K. D., Ferguson, D. O., & Alt, F. W. (2003). The role of DNA breaks in genomic instability and tumorigenesis. Immunological Reviews, 194, 77–94.PubMedGoogle Scholar
  81. Milton, C. C., Huynh, B., Batterham, P., Rutherford, S. L., & Hoffmann, A. A. (2003). Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of canalization and developmental stability. Proceedings of National Academy of Sciences of the United States of America, 100, 13396–13401.Google Scholar
  82. Mohrenweiser, H. W., Wilson, D. M., & Jones, I. M. (2003). Challenges and complexities in estimating both the functional impact and the disease risk associated with the extensive genetic variation in human DNA repair genes. Mutation Research, 526, 93–125.PubMedGoogle Scholar
  83. Moran, P. A. P. (1992). The evolutionary maintenance of alternative phenotypes. American Naturalist, 139, 971–989.Google Scholar
  84. Moro, G. L., Habben, J. E., Hamaker, B. R., & Larkins, B. A. (1996). Characterization of the variability in lysine content for normal and opaque2 maize endosperm. Crop Science, 36, 1651–1659.CrossRefGoogle Scholar
  85. Moss, M. (1971). Functional cranial analysis and the functional matrix. American Speech Hearing Association Report, 6, 5–18.Google Scholar
  86. Moss, M., & Young, R. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281–292.PubMedGoogle Scholar
  87. Nijhout, F. H. (1999). Control mechanisms of polyphonic development in insects. BioScience, 49, 181–192.Google Scholar
  88. Nijhout, H. F., & Davidowitz, G. (2003). Developmental perspectives on phenotypic variation: canalization, and fluctuating asymmetry. In: M. Polak (Ed.), Developmental instability (DI): Causes and consequences (pp. 3–13). Oxford: Oxford University Press.Google Scholar
  89. Nilsson-Ehle, H. (1914). Vilka erfarenheter hava hittills vunnits rörande möjligheten av växters acklimatisering? Kungl Landtbruksakad Hand Tidskr, 53, 537–572.Google Scholar
  90. Olson, E. C., & Miller, R. L. (1951). A mathematical model applied to a study of the evolution of species. Evolution, 5, 256–338.Google Scholar
  91. Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.Google Scholar
  92. Palmer, A. R. (1996). Waltzing with asymmetry. BioScience, 46, 518–532.Google Scholar
  93. Palmer, A. R., & Strobeck, C. (1986). Fluctuating Asymmetry: Measurement, Analysis, Patterns. Annual Review Ecology Systematics, 17, 391–421.Google Scholar
  94. Palmer, A. R., & Strobeck, C. (1992). Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zoologica Fennica, 191, 57–72.Google Scholar
  95. Palmer, R., & Strobeck, C. (2003). Fluctuating asymmetry analysis unplugged. In: M. Polak (Ed.), Developmental instability (DI): Causes and consequences (pp. 279–319). Oxford: Oxford University Press.Google Scholar
  96. Qiu, M., Bulfone, A., Ghattas, I., Meneses, J. J., Christensen, L., Sharpe, P. T., Presley, R., Pederson, R. A., & Rubenstein, J. L. R. (1997). Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: Mutations of Dlx-1, Dlx-2 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from first and second arches. Developmental Biology, 185, 165–184.PubMedGoogle Scholar
  97. Rafferty, K. L., Herring, S. W., & Artese, F. (2000). Three-dimensional loading and growth of the zygomatic arch. Journal of Experimental Biology, 203, 2093–3004.PubMedGoogle Scholar
  98. Rasmuson, M. (2002). Fluctuating asymmetry—indicator of what? Hereditas, 136, 177–183.PubMedGoogle Scholar
  99. Réale, D., & Roff, D. A. (2003). Inbreeding, developmental stability, and canalization in the sand cricket Gryllus firmus. Evolution, 57, 597–605.PubMedGoogle Scholar
  100. Reeve, E. C. R. 1960. Some genetic tests on asymmetry of sternopleural chaetae number in Drosophila. Genetical Research, 1, 151–172.CrossRefGoogle Scholar
  101. Reeve, E. C. R., & Robertson, F. W. (1953). Analysis of environmental variability in quantitative inheritance. Nature, 171, 874–875.PubMedGoogle Scholar
  102. Rendel, J. M. (1959). Canalization of the scute phenotype of Drosophila. Evolution, 13, 425–439.Google Scholar
  103. Richtsmeier, J. T., Aldridge, K. A., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., Yan, P., Cole, T. M., III. 2006. Phenotypic integration of neurocranium and brain. Journal of Experimental Zoology (Molecular and Development Evolution), 306B, 1–19.Google Scholar
  104. Routman, E. J., & Cheverud, J. M. (1997). Gene effects on a quantitative trait: two-locus epistatic effects measured at microsatellite markers and at estimated QTL. Evolution, 51, 1654–1662.Google Scholar
  105. Rutherford, S. L. (2000). From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays, 22, 1095–1105.PubMedGoogle Scholar
  106. Rutherford, S. L., & Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396, 336–342.PubMedGoogle Scholar
  107. Salazar-Ciudad, I., Newman, S. A., Solé RV. 2001a. Phenotypic and dynamical transitions in model genetic networks I. Emergence of patterns and genotype–phenotype relations. Evolution & Development, 3, 84–94.Google Scholar
  108. Salazar-Ciudad, I., Solé RV, Newman SA. 2001b. Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms. Evolution & Development, 3, 95–103.Google Scholar
  109. Salazar-Ciudad, I., & Jernvall, J. (2002). A gene network model accounting for development and evolution of mammalian teeth. Proceedings of National Academy of Sciences of the United States of America, 99, 8116–8120.Google Scholar
  110. Salazar-Ciudad, I., & Jernvall, J. (2004). How different types of pattern formation mechanisms affect the evolution of form and development. Evolution & Development, 6, 6–16.Google Scholar
  111. Salazar-Ciudad, I., & Jernvall, J. (2005). Graduality and innovation in the evolution of complex phenotypes: Insights from development. Journal of Experimental Zoology (Molecular and Development Evolution), 304B, 619–631.Google Scholar
  112. Santos, M., Fernández Iriarte, P., & Céspedes, W. (2005). Genetics and geometry of canalization and developmental stability in Drosophila subobscura. BMC Evolutionary Biology, 5, 7.PubMedGoogle Scholar
  113. Scharloo, W. (1991). Canalization: Genetic and developmental aspects. Annual Review of Ecology Systematics, 22, 65–93.Google Scholar
  114. Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology Systematics, 24, 35–68.Google Scholar
  115. Schlichting, C. D. (1986). The evolution of phenotypic plasticity in plants. Annual Review of Ecology Systematics, 17, 667–693.Google Scholar
  116. Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland MA: Sinauer.Google Scholar
  117. Schmalhausen, I. I. (1949). Factors of evolution. Chicago: University of Chicago Press.Google Scholar
  118. Siegal, M. L., & Bergman, A. (2002). Waddington’s canalization revisited: developmental stability and evolution. Proceedings of National Academy of Sciences of the United States of America, 99, 10528–10532.Google Scholar
  119. Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. BioScience, 39, 436–445.Google Scholar
  120. Stock, D. W. (2005). The Dlx complement of the leopard shark, Triakis semifasciata, resembles that of mammals: Implications for genomic and morphological evolution of jawed vertebrates. Genetics, 169, 807–817.PubMedGoogle Scholar
  121. Suzuki, D. T., Griffiths, A. J. F., Miller, J. H., & Lewontin, R. C. (1986). An introduction to genetic analysis. New York: WH Freeman.Google Scholar
  122. Thomas, J. H. (1993). Thinking about genetic redundancy. Trends in Genetics, 9, 305–309.Google Scholar
  123. Thorogood, P. (1983). Morphogenesis of cartilage. In: B. K. Hall (Ed.), Cartilage, development, differentiation and growth. Vol. 2. (pp. 223–255). New York: Academic Press.Google Scholar
  124. Turman, J. E., Jr. 2007. The development of mastication in rodents: From neurons to behaviors. Archives of Oral Biology, 52, 313–316.PubMedGoogle Scholar
  125. Van Dongen, S. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. Journal of Evolutionary Biology, 19, 1727–1743.PubMedGoogle Scholar
  126. Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution, 16, 125–142.Google Scholar
  127. von Dassow, G., Meir, E., Munro, E., & Odell, G. (2000). The segment polarity network is a robust development module. Nature, 406, 188–192.Google Scholar
  128. Waddington, C. H. (1942). The canalisation of development and the inheritance of acquired characters. Nature, 150, 563.Google Scholar
  129. Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution, 7, 118–126.Google Scholar
  130. Waddington, C. H. (1956). Genetic assimilation of the bithorax phenotype. Evolution, 10, 1–13.Google Scholar
  131. Waddington, C. H. (1957). Strategy of the genes. New York: MacMillan.Google Scholar
  132. Waddington, C. H. (1959). Canalization of development and genetic assimilation of acquired characters. Nature, 183, 1654–1655.PubMedGoogle Scholar
  133. Waddington, C. H. (1961). Genetic assimilation. Advances in Genetics, 10, 257–293.PubMedCrossRefGoogle Scholar
  134. Waddington, C. H. (1975). The Evolution of an evolutionist. Ithaca, New York: Cornell University Press.Google Scholar
  135. Wagner, A. (1999). Redundant gene functions and natural selection. Journal of Evolutionary Biology, 12, 1–16.Google Scholar
  136. Wagner, A. (2005). Distributed robustness versus redundancy as causes of mutational robustness. BioEssays, 27, 176–188.PubMedGoogle Scholar
  137. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.Google Scholar
  138. Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50, 967–976.Google Scholar
  139. Wagner, G. P., Booth, G., Bagheri-Chaichian, H. 1997. A population genetic theory of canalization. Evolution, 51, 329–347.Google Scholar
  140. Wagner, G. P., Laubichle, MD, Bagheri-Chaichian, H. (1998). Genetic measurement theory of epistatic effects. Genetica, 102–103, 569–580.PubMedGoogle Scholar
  141. Weiss, K. M., & Fullerton, S. M. (2000). Phenogenetic drift and the evolution of genotype–phenotype relations. Theoretical Population Biology, 57, 187–195.PubMedGoogle Scholar
  142. Weiss, K. M., & Buchanan, A. V. (2004). Genetics and The logic of Evolution. New York: John Wiley.Google Scholar
  143. Weiss, P. A. (1971). The basic concept of hierarchic systems. In: P. A. Weiss (Ed.), Hierarchically organized systems in theory and practice (pp. 1–43.). New York: Hafner Publishing Company.Google Scholar
  144. West-Eberhard, M. J. (1986). Alternative adaptations, speciation, and phylogeny. Proceedings of National Academy of Sciences of the United States of America, 83, 1388–1392.Google Scholar
  145. West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press.Google Scholar
  146. West-Eberhard, M. J. (2005). Phenotypic accommodation: Adaptive innovation due to developmental plasticity. Journal of Experimental Zoology (Molecular and Development Evolution), 304B, 610–618.Google Scholar
  147. Willmore, K. E., Klingenberg, C. P., Hallgrímsson, B. 2005. The relationship between fluctuating asymmetry and environmental variance in Rhesus macaque skulls. Evolution, 59, 898–909.PubMedGoogle Scholar
  148. Willmore, K. E., Hallgrímsson, B. (2005). Within individual variation: Developmental noise versus developmental stability. In: B. Hallgrímsson, & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 191–218). New York: Elsevier Academic Press.Google Scholar
  149. Willmore, K. E., Leamy, L., Hallgrímsson, B. (2006). Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution & Development, 8, 550–567.Google Scholar
  150. Woltereck, R. (1909). Weitere experimentelle untersuchungen über artveränderung, speziell über das wesen quantitaver artunterschiede bei Daphnien. Verh Deutsch Zool Gesellsch, 19, 110–173.Google Scholar
  151. Woods, R. E., Sgrò CM, Hercus, M. J., & Hoffmann, A. A. (1999). The association between fluctuating asymmetry, trait variability, trait heritability, and stress: A multiply replicated experiment on combined stresses in Drosophila melanogaster. Evolution, 53, 493–505.Google Scholar
  152. Yamada, K., & Kimmel, D. B. (1991). The effect of dietary consistency on bone mass and turnover in the growing rat mandible. Archives of Oral Biology, 36, 129–138.PubMedGoogle Scholar
  153. Young, N. M. (2006). Function, ontogeny and canalization of shape vairance in the primate scapula. Journal of Anatomy, 209, 623–636.PubMedGoogle Scholar
  154. Young, N. M., Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59, 2691–2704.PubMedGoogle Scholar
  155. Zakharaov, V. M. (1992). Population phenotgenetics: analysis of developmental stability in natural populations. Acta Zoologica Fennica, 191, 7–30.Google Scholar
  156. Zelditch, M. L., Bookstein, F. L., & Lundrigan, B. L. (1993). The ontogenetic complexity of developmental constraints. Journal of Evolutionary Biology, 6, 621–641.Google Scholar
  157. Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution & Development, 6, 194–206.Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Katherine Elizabeth Willmore
    • 1
  • Nathan M. Young
    • 2
  • Joan T. Richtsmeier
    • 1
  1. 1.Department of AnthropologyPennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Orthopaedic SurgeryUniversity of California at San FranciscoSan FranciscoUSA

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