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Phenotypic Variability: Its Components, Measurement and Underlying Developmental Processes

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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.

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References

  • Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101–157.

    PubMed  CAS  Google Scholar 

  • 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 

  • Bagheri, H. C., & Wagner, G. P. (2004). Evolution of dominance in metabolic pathways. Genetics, 168, 1713–1735.

    PubMed  CAS  Google Scholar 

  • Berg, R. L. (1959). The ecological significance of correlational pleiades. Evolution, 14, 171–180.

    Google Scholar 

  • Bjorksten, T. A., Fowler, K., & Pomiankowski, A. (2000). What does sexual trait FA tell us about stress? TREE, 15, 163–166.

    PubMed  Google Scholar 

  • Blake, W. J., Kaern, M., Cantor, C. R., & Collins, J. J. (2003). Noise in eukaryotic gene expression. Nature, 422, 633–637.

    PubMed  CAS  Google Scholar 

  • Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics, 13, 115–155.

    Google Scholar 

  • Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868–873.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499–516.

    Google Scholar 

  • Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155–171.

    PubMed  CAS  Google Scholar 

  • Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42, 958–968.

    Google Scholar 

  • Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145, 63–89.

    Google Scholar 

  • Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.

    Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Clarke, G. M. (1993). The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica, 89, 15–23.

    Google Scholar 

  • Clarke, G. M. (1998). The genetic basis of developmental stability, V. Inter- and intra-individual character variation. Heredity, 80, 562–567.

    Google Scholar 

  • 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.

  • 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 

  • Cottrill, C. P., Archer, C. W., & Wolpert, L. (1987). Cell sorting and chongrogenic aggregate formation in micromass culture. Developmental Biology, 122, 503–515.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Depew, M. J., Lufkin, T., & Rubenstein, J. L. R. (2002). Specification of jaw subdivisions by Dlx genes. Science, 298, 381–385.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Dunn, R. B., & Fraser, A. S. (1958). Selection for an invariant character—“vibrissae number”—in the house mouse. Nature, 181, 1018–1019.

    Google Scholar 

  • 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 

  • Eccleston, A, DeWitt, N., Gunter, C., Marte B., & Nath, D. (2007). Epigenetics. Nature, 447, 395.

    CAS  Google Scholar 

  • 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 

  • 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 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. New York: Longman Press.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gibson, G., & van Helden, S. (1997). Is function of the Drosophila homeotic gene Ultrabithorax canalized? Genetics, 147, 1155–1168.

    PubMed  CAS  Google Scholar 

  • Gibson, G., & Wagner, G. (2000). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372–380.

    PubMed  CAS  Google Scholar 

  • Gilbert, S. F. (2003). Developmental biology (7th ed.) Massachusetts: Sinauer Associated Inc.

    Google Scholar 

  • 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 

  • Graham, A. (2002). Jaw development: Chinless wonders. Current Biology, 12, 810–812.

    Google Scholar 

  • 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 

  • 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 

  • Hall, B. K. (1978). Developmental and cellular skeletal biology. New York: Academic Press.

    Google Scholar 

  • Hall, B. K. (1988). The embryonic development of bone. American Scientist, 76, 174–181.

    Google Scholar 

  • Hall, B. K. (1999). The neural crest in development and evolution. New York: Springer-Verlag.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hermisson, J., & Wagner, G. P. (2004). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372–380.

    Google Scholar 

  • 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 

  • Herring, S. W., & Teng, S. (2000). Strain in the braincase and its sutures during function. American Journal of Physical Anthropology, 112, 575–593.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Houle, D. (1998). How should we explain variation in genetic variance of traits? Genetica, 102/103, 241–253.

    Google Scholar 

  • Huerta-Sanchez, E., & Durrett, R. (2007). Wagner’s canalization model. Theoretical Population Biology, 71, 121–130.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Jacob, F. (1977). Evolution and tinkering. Science, 196, 1161–1166.

    PubMed  CAS  Google Scholar 

  • 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 

  • Johnson, D. R. (1986). The genetics of the skeleton. Oxford: Clarendon Press.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Kaufmann, W. K., & Paules, R. S. (1996). DNA damage and cell cycle checkpoints. The FASEB Journal, 10, 238–247.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Klingenberg, C. P., & Zaklan, S. D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54, 1273–1285.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kuratani, S. (2005). Developmental studies of the lamprey and hierarchical evolutionary steps towards the acquisition of the jaw. Journal of Anatomy, 207, 489–499.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Ludwig, W. (1932). Das Rechts-links problem im Teirreich und beim Menschen. Berlin (Germany): Springer.

    Google Scholar 

  • Lund, J. P., & Kolta, A. (2006). Generation of the central masticatory pattern and its modification by sensory feedback. Dysphagia, 21, 167–174.

    PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Moran, P. A. P. (1992). The evolutionary maintenance of alternative phenotypes. American Naturalist, 139, 971–989.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Moss, M. (1971). Functional cranial analysis and the functional matrix. American Speech Hearing Association Report, 6, 5–18.

    Google Scholar 

  • Moss, M., & Young, R. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281–292.

    PubMed  CAS  Google Scholar 

  • Nijhout, F. H. (1999). Control mechanisms of polyphonic development in insects. BioScience, 49, 181–192.

    Google Scholar 

  • 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 

  • Nilsson-Ehle, H. (1914). Vilka erfarenheter hava hittills vunnits rörande möjligheten av växters acklimatisering? Kungl Landtbruksakad Hand Tidskr, 53, 537–572.

    Google Scholar 

  • 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 

  • Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.

    Google Scholar 

  • Palmer, A. R. (1996). Waltzing with asymmetry. BioScience, 46, 518–532.

    Google Scholar 

  • Palmer, A. R., & Strobeck, C. (1986). Fluctuating Asymmetry: Measurement, Analysis, Patterns. Annual Review Ecology Systematics, 17, 391–421.

    Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Rasmuson, M. (2002). Fluctuating asymmetry—indicator of what? Hereditas, 136, 177–183.

    PubMed  Google Scholar 

  • Réale, D., & Roff, D. A. (2003). Inbreeding, developmental stability, and canalization in the sand cricket Gryllus firmus. Evolution, 57, 597–605.

    PubMed  Google Scholar 

  • Reeve, E. C. R. 1960. Some genetic tests on asymmetry of sternopleural chaetae number in Drosophila. Genetical Research, 1, 151–172.

    Article  Google Scholar 

  • Reeve, E. C. R., & Robertson, F. W. (1953). Analysis of environmental variability in quantitative inheritance. Nature, 171, 874–875.

    PubMed  CAS  Google Scholar 

  • Rendel, J. M. (1959). Canalization of the scute phenotype of Drosophila. Evolution, 13, 425–439.

    Google Scholar 

  • 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 

  • 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 

  • Rutherford, S. L. (2000). From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays, 22, 1095–1105.

    PubMed  CAS  Google Scholar 

  • Rutherford, S. L., & Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396, 336–342.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • Santos, M., Fernández Iriarte, P., & Céspedes, W. (2005). Genetics and geometry of canalization and developmental stability in Drosophila subobscura. BMC Evolutionary Biology, 5, 7.

    PubMed  Google Scholar 

  • Scharloo, W. (1991). Canalization: Genetic and developmental aspects. Annual Review of Ecology Systematics, 22, 65–93.

    Google Scholar 

  • Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology Systematics, 24, 35–68.

    Google Scholar 

  • Schlichting, C. D. (1986). The evolution of phenotypic plasticity in plants. Annual Review of Ecology Systematics, 17, 667–693.

    Google Scholar 

  • Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland MA: Sinauer.

    Google Scholar 

  • Schmalhausen, I. I. (1949). Factors of evolution. Chicago: University of Chicago Press.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. BioScience, 39, 436–445.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Thomas, J. H. (1993). Thinking about genetic redundancy. Trends in Genetics, 9, 305–309.

    Google Scholar 

  • 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 

  • Turman, J. E., Jr. 2007. The development of mastication in rodents: From neurons to behaviors. Archives of Oral Biology, 52, 313–316.

    PubMed  Google Scholar 

  • Van Dongen, S. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. Journal of Evolutionary Biology, 19, 1727–1743.

    PubMed  CAS  Google Scholar 

  • Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution, 16, 125–142.

    Google Scholar 

  • 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 

  • Waddington, C. H. (1942). The canalisation of development and the inheritance of acquired characters. Nature, 150, 563.

    Google Scholar 

  • Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution, 7, 118–126.

    Google Scholar 

  • Waddington, C. H. (1956). Genetic assimilation of the bithorax phenotype. Evolution, 10, 1–13.

    Google Scholar 

  • Waddington, C. H. (1957). Strategy of the genes. New York: MacMillan.

    Google Scholar 

  • Waddington, C. H. (1959). Canalization of development and genetic assimilation of acquired characters. Nature, 183, 1654–1655.

    PubMed  CAS  Google Scholar 

  • Waddington, C. H. (1961). Genetic assimilation. Advances in Genetics, 10, 257–293.

    Article  PubMed  CAS  Google Scholar 

  • Waddington, C. H. (1975). The Evolution of an evolutionist. Ithaca, New York: Cornell University Press.

    Google Scholar 

  • Wagner, A. (1999). Redundant gene functions and natural selection. Journal of Evolutionary Biology, 12, 1–16.

    Google Scholar 

  • Wagner, A. (2005). Distributed robustness versus redundancy as causes of mutational robustness. BioEssays, 27, 176–188.

    PubMed  CAS  Google Scholar 

  • Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50, 967–976.

    Google Scholar 

  • Wagner, G. P., Booth, G., Bagheri-Chaichian, H. 1997. A population genetic theory of canalization. Evolution, 51, 329–347.

    Google Scholar 

  • Wagner, G. P., Laubichle, MD, Bagheri-Chaichian, H. (1998). Genetic measurement theory of epistatic effects. Genetica, 102–103, 569–580.

    PubMed  Google Scholar 

  • Weiss, K. M., & Fullerton, S. M. (2000). Phenogenetic drift and the evolution of genotype–phenotype relations. Theoretical Population Biology, 57, 187–195.

    PubMed  CAS  Google Scholar 

  • Weiss, K. M., & Buchanan, A. V. (2004). Genetics and The logic of Evolution. New York: John Wiley.

    Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Young, N. M. (2006). Function, ontogeny and canalization of shape vairance in the primate scapula. Journal of Anatomy, 209, 623–636.

    PubMed  Google Scholar 

  • Young, N. M., Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59, 2691–2704.

    PubMed  Google Scholar 

  • Zakharaov, V. M. (1992). Population phenotgenetics: analysis of developmental stability in natural populations. Acta Zoologica Fennica, 191, 7–30.

    Google Scholar 

  • 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 

  • 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 

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Acknowledgements

We thank Miriam Zelditch, David Polly and an anonymous reviewer for their insightful comments on a previous draft of this paper. We also thank Benedikt Hallgrímsson and the members of the Richtsmeier laboratory for their willingness to discuss these issues at great length and for their many helpful suggestions. This work was supported by the National Science Foundation grant BCS-0523637, as well as the William H. Davies Student Fellowship, Medical Science Graduate Research Fellowship, University of Calgary Graduate Studies (to KW).

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Glossary

Buffering

any mechanism that limits the phenotypic effects of a perturbation whether it is adaptive or not.

Canalization

refers to the property of an organism that ensures similarity of phenotypic expression by buffering development against both environmental and genetic perturbations.

Developmental instability

the inverse of developmental stability.

Developmental noise

minor environmentally induced developmental accidents.

Developmental stability

the property of an organism that buffers variation of micro-environmental origin. That is, developmental stability ensures consistent phenotypic expression within individuals, or within a given genotype and environment.

Environmental canalization

refers to the limitation of phenotypic effect caused by exposure to environmental change.

Epigenetics

heritable changes in gene expression that are not due to changes in DNA sequence.

Fluctuating asymmetry (FA)

random, non-directional deviations from symmetry of bilaterally symmetric traits such as limbs, wings or antennae. FA measures the balance between developmental noise and developmental stability.

Genetic architecture

refers to the number of genes and the interactions between them whose products govern a particular trait.

Genetic canalization

refers to the robustness of the phenotype to the effects of mutation.

Module

a character, or a set of characters that are more tightly integrated internally than they are with other characters.

Morphological integration

refers to the inter-relatedness between morphological structures often due to common developmental origins or functional demands.

Norm of reaction

the range of expected phenotypes under a given set of environmental and genetic conditions.

Perturbation

used here as any disruption to development. Could be genetic, developmental, environmental, or adverse interactions between these factors.

Phenotypic plasticity

phenotypic variation induced by the environement.

Pleiotropy

the control of one gene on multiple traits.

Stabilizing selection

most common form of natural selection, selects for the mean phenotype.

Variability

a dispositional term like solubility describing the tendency or propensity to vary.

Variation

observed phenotypic differences.

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Willmore, K.E., Young, N.M. & Richtsmeier, J.T. Phenotypic Variability: Its Components, Measurement and Underlying Developmental Processes. Evol Biol 34, 99–120 (2007). https://doi.org/10.1007/s11692-007-9008-1

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