Skip to main content

Advertisement

Log in

Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation

  • Synthesis Paper
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Organisms represent a complex arrangement of anatomical structures and individuated parts that must maintain functional associations through development. This integration of variation between functionally related body parts and the modular organization of development are fundamental determinants of their evolvability. This is because integration results in the expression of coordinated variation that can create preferred directions for evolutionary change, while modularity enables variation in a group of traits or regions to accumulate without deleterious effects on other aspects of the organism. Using our own work on both model systems (e.g., lab mice, avians) and natural populations of rodents and primates, we explore in this paper the relationship between patterns of phenotypic covariation and the developmental determinants of integration that those patterns are assumed to reflect. We show that integration cannot be reliably studied through phenotypic covariance patterns alone and argue that the relationship between phenotypic covariation and integration is obscured in two ways. One is the superimposition of multiple determinants of covariance in complex systems and the other is the dependence of covariation structure on variances in covariance-generating processes. As a consequence, we argue that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Ackermann, R. R., & Cheverud, J. M. (2000). Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlation and common principal component analysis. American Journal of Physical Anthropology, 111(4), 489–501.

    CAS  PubMed  Google Scholar 

  • Alberch, P. (1982). Developmental constraints in evolutionary processes. In J. T. Bonner (Ed.), Development in evolution (pp. 313–332). Berlin and New York: Springer.

    Google Scholar 

  • Ballock, R. T., & O’Keefe, R. J. (2003). The biology of the growth plate. Journal of Bone and Joint Surgery—American Volume, 85-A(4), 715–726.

    Google Scholar 

  • Bastir, M., Rosas, A., & O’Higgins, P. (2006). Craniofacial levels and the morphological maturation of the human skull. Journal of Anatomy, 209(5), 637–654.

    PubMed  Google Scholar 

  • Blechschmidt, I. E. (1961). The stages of human development before birth. An introduction to human embryology. Basel: Karger Medical Publishers.

    Google Scholar 

  • Bookstein, F. L. (1991). Morphometric tools for landmark data. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bookstein, F. L., Gunz, P., Mitteroecker, P., Prossinger, H., Schaefer, K., & Seidler, H. (2003). Cranial integration in Homo: Singular warps analysis of the midsagittal plane in ontogeny and evolution. Journal of Human Evolution, 44(2), 167–187.

    PubMed  Google Scholar 

  • Boughner, J. C., & Hallgrímsson, B. (2008). Biological spacetime and the temporal integration of functional modules: A case study of dento-gnathic developmental timing. Developmental Dynamics, 237(1), 1–17.

    PubMed  Google Scholar 

  • Boughner, J. C., Wat, S., Diewert, V. M., Young, N. M., Browder, L. W., & Hallgrímsson, B. (2008). Short-faced mice and developmental interactions between the brain and the face. Journal of Anatomy, 213(6), 646–662.

    PubMed  Google Scholar 

  • Burger, R. (1986). Evolutionary dynamics of functionally constrained phenotypic characters. IMA Journal of Mathematics Applied in Medicine and Biology, 3(4), 265–287.

    CAS  PubMed  Google Scholar 

  • Capdevila, J., & Izpisua Belmonte, J. C. (2001). Patterning mechanisms controlling vertebrate limb development. Annual Review of Cell and Developmental Biology, 17, 87–132.

    CAS  PubMed  Google Scholar 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental 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.

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Cortes, M., Baria, A. T., & Schwartz, N. B. (2009). Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development, 136(10), 1697–1706.

    CAS  PubMed  Google Scholar 

  • Cox, T. C. (2004). Taking it to the max: The genetic and developmental mechanisms coordinating midfacial morphogenesis and dysmorphology. Clinical Genetics, 65(3), 163–176.

    CAS  PubMed  Google Scholar 

  • Diewert, V. M., & Lozanoff, S. (1993). Growth and morphogenesis of the human embryonic midface during primary palate formation analyzed in frontal sections. Journal of Craniofacial Genetics and Developmental Biology, 13(3), 162–183.

    CAS  PubMed  Google Scholar 

  • Diez, M., Schweinhardt, P., Petersson, S., Wang, F. H., Lavebratt, C., Schalling, M., et al. (2003). MRI and in situ hybridization reveal early disturbances in brain size and gene expression in the megencephalic (mceph/mceph) mouse. European Journal of Neuroscience, 18(12), 3218–3230.

    PubMed  Google Scholar 

  • Donahue, L. R., Cook, S. A., Johnson, K. R., Bronson, R. T., & Davisson, M. T. (1996). Megencephaly: A new mouse mutation on chromosome 6 that causes hypertrophy of the brain. Mammalian Genome, 7(12), 871–876.

    CAS  PubMed  Google Scholar 

  • Downey, C. M., Horton, C. R., Carlson, B. A., Parsons, T. E., Hatfield, D. L., Hallgrímsson, B., et al. (2009). Osteo-chondroprogenitor-specific deletion of the selenocysteine tRNA gene, Trsp, leads to chondronecrosis and abnormal skeletal development: A putative model for Kashin-Beck disease. PLoS Genetics, 5(8), e1000616.

    PubMed  Google Scholar 

  • Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.

    Google Scholar 

  • Eberhart, J. K., Swartz, M. E., Crump, J. G., & Kimmel, C. B. (2006). Early Hedgehog signaling from neural to oral epithelium organizes anterior craniofacial development. Development, 133(6), 1069–1077.

    CAS  PubMed  Google Scholar 

  • Fischer-Rousseau, L., Cloutier, R., & Zelditch, M. L. (2009). Morphological integration and developmental progress during fish ontogeny in two contrasting habitats. Evolution and Development, 11(6), 740–753.

    PubMed  Google Scholar 

  • Ford-Hutchinson, A. F., Ali, Z., Lines, S. E., Hallgrímsson, B., Boyd, S. K., & Jirik, F. R. (2007). Inactivation of Pten in osteo-chondroprogenitor cells leads to epiphyseal growth plate abnormalities and skeletal overgrowth. Journal of Bone and Mineral Research, 22(8), 1245–1259.

    CAS  PubMed  Google Scholar 

  • Ford-Hutchinson, A. F., Ali, Z., Seerattan, R. A., Cooper, D. M., Hallgrímsson, B., Salo, P. T., et al. (2005). Degenerative knee joint disease in mice lacking 3′-phosphoadenosine 5′-phosphosulfate synthetase 2 (Papss2) activity: A putative model of human PAPSS2 deficiency-associated arthrosis. Osteoarthritis and Cartilage, 13(5), 418–425.

    PubMed  Google Scholar 

  • Gibson-Brown, J. J., Agulnik, S. I., Chapman, D. L., Alexiou, M., Garvey, N., Silver, L. M., et al. (1996). Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mechanisms of Development, 56, 93–101.

    CAS  PubMed  Google Scholar 

  • Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40(1), 33–51.

    Google Scholar 

  • Griswold, C. K. (2006). Pleiotropic mutation, modularity and evolvability. Evolution and Development, 8, 81–93.

    PubMed  Google Scholar 

  • Gunz, P., & Harvati, K. (2007). The Neanderthal “chignon”: Variation, integration, and homology. Journal of Human Evolution, 52(3), 262–274.

    PubMed  Google Scholar 

  • Hagstrom, K. A., & Meyer, B. J. (2003). Condensin and cohesin: More than chromosome compactor and glue. Nature Reviews. Genetics, 4(7), 520–534.

    CAS  PubMed  Google Scholar 

  • Hall, B. K. (1999). Evolutionary developmental biology. Dordrecht: Kluwer.

    Google Scholar 

  • Hallgrímsson, B., Brown, J. J. Y., Ford-Hutchinson, A. F., Sheets, H. D., Zelditch, M. L., & Jirik, F. R. (2006). The brachymorph mouse and the developmental-genetic basis for canalization and morphological integration. Evolution & Development, 8(1), 61–73.

    Google Scholar 

  • Hallgrímsson, B., Dorval, C. J., Zelditch, M. L., & German, R. Z. (2004a). Craniofacial variability and morphological integration in mice susceptible to cleft lip and palate. Journal of Anatomy, 205(6), 501–517.

    PubMed  Google Scholar 

  • Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48(3), 373–384.

    Google Scholar 

  • Hallgrímsson, B., Lieberman, D. E., Liu, W., Ford-Hutchinson, A. F., & Jirik, F. R. (2007a). Epigenetic interactions and the structure of phenotypic variation in the cranium. Evolution and Development, 9(1), 76–91.

    PubMed  Google Scholar 

  • Hallgrímsson, B., Lieberman, D. E., Young, N. M., Parsons, T., & Wat, S. (2007b). Evolution of covariance in the mammalian skull. Novartis Foundation Symposium, 284, 164–185; discussion 185–190.

    Google Scholar 

  • Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. (2004b). Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 302(3), 207–225.

    PubMed  Google Scholar 

  • Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology, 45, 131–158.

    Google Scholar 

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.

    CAS  PubMed  Google Scholar 

  • Hansen, T., Pélabon, C., & Armbruster, W. (2007). Comparing variational properties of homologous floral and vegetative characters in Dalechampia scandens: Testing the berg hypothesis. Evolutionary Biology, 34(1), 86–98.

    Google Scholar 

  • Hendrikse, J. L., Parsons, T. E., & Hallgrímsson, B. (2007). Evolvability as the proper focus of evolutionary developmental biology. Evolution and Development, 9(4), 393–401.

    PubMed  Google Scholar 

  • Hinchliffe, J. R., & Johnson, D. R. (1980). The development of the vertebrate limb. New York and London: Oxford University Press.

    Google Scholar 

  • Hu, D., & Marcucio, R. S. (2009a). A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development, 136(1), 107–116.

    CAS  PubMed  Google Scholar 

  • Hu, D., & Marcucio, R. S. (2009b). Unique organization of the frontonasal ectodermal zone in birds and mammals. Developmental Biology, 325(1), 200–210.

    CAS  PubMed  Google Scholar 

  • Hu, D., Marcucio, R. S., & Helms, J. A. (2003). A zone of frontonasal ectoderm regulates patterning and growth in the face. Development, 130(9), 1749–1758.

    CAS  PubMed  Google Scholar 

  • Jamniczky, H. A., & Hallgrímsson, B. (2009). A comparison of covariance structure in wild and laboratory muroid crania. Evolution, 63(6), 1540–1556.

    PubMed  Google Scholar 

  • Jones, A. G., Arnold, S. J., & Burger, R. (2007). The mutation matrix and the evolution of evolvability. Evolution: International Journal of Organic Evolution, 61(4), 727–745.

    Google Scholar 

  • Juriloff, D. M., Harris, M. J., & Brown, C. J. (2001). Unravelling the complex genetics of cleft lip in the mouse model. Mammalian Genome, 12(6), 426–435.

    CAS  PubMed  Google Scholar 

  • Juriloff, D. M., Harris, M. J., McMahon, A. P., Carroll, T. J., & Lidral, A. C. (2006). Wnt9b is the mutated gene involved in multifacial nonsyndromic cleft lip with or without cleft palate in A/WySn mice, as confirmed by a genetic complementation test. Birth Defects Research (Part A): Clinical and Molecular Teratology, 76, 574–579.

    CAS  Google Scholar 

  • Kawauchi, S., Calof, A. L., Santos, R., Lopez-Burks, M. E., Young, C. M., Hoang, M. P., et al. (2009). Multiple organ system defects and transcriptional dysregulation in the Nipbl(±) mouse, a model of Cornelia de Lange Syndrome. PLoS Genetics, 5(9), e1000650.

    PubMed  Google Scholar 

  • Kember, N. F. (1993). Cell kinetics and the control of bone growth. Acta Paediatrica, 82(Suppl 391):61–65.

    Google Scholar 

  • Kirkwood, J., & Kember, N. (1993). Comparative quantitative histology of mammalian growth plates. Journal of Zoology, 231, 543–562.

    Google Scholar 

  • Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology and Systematics, 39, 115–132.

    Google Scholar 

  • Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405–421.

    Google Scholar 

  • Klingenberg, C. P., & Nijhout, H. F. (1999). Genetics of fluctuating asymmetry: A developmental model of developmental instability. Evolution, 53(2), 358–375.

    Google Scholar 

  • Kristensen, E., Parsons, T. E., Hallgrímsson, B., & Boyd, S. K. (2008). A novel 3-D image-based morphological method for phenotypic analysis. IEEE Transactions on Biomedical Engineering, 55(12), 2826–2831.

    PubMed  Google Scholar 

  • Lieberman, D. E., Hallgrímsson, B., Liu, W., Parsons, T. E., & Jamniczky, H. A. (2008). Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: Testing a new model using mice. Journal of Anatomy, 212(6), 720–735.

    PubMed  Google Scholar 

  • Lieberman, D. E., McBratney, B. M., & Krovitz, G. (2002). The evolution and development of cranial form in Homo Sapiens. PNAS, 99(3), 1134–1139.

    CAS  PubMed  Google Scholar 

  • Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000). Basicranial influence on overall cranial shape. Journal of Human Evolution, 38(2), 291–315.

    CAS  PubMed  Google Scholar 

  • Love, A. (2006). Evolutionary morphology and Evo-devo: Hierarchy and novelty. Theory in Biosciences, 124(3), 317–333.

    PubMed  Google Scholar 

  • Maeda, Y., Nakamura, E., Nguyen, M. T., Suva, L. J., Swain, F. L., Razzaque, M. S., et al. (2007). Indian Hedgehog produced by postnatal chondrocytes is essential for maintaining a growth plate and trabecular bone. Proceedings of the National Academy of Sciences of the United States of America, 104(15), 6382–6387.

    CAS  PubMed  Google Scholar 

  • Magwene, P. M. (2001). New tools for studying integration and modularity. Evolution, 55(9), 1734–1745.

    CAS  PubMed  Google Scholar 

  • Marcucio, R. S., Cordero, D. R., Hu, D., & Helms, J. A. (2005). Molecular interactions coordinating the development of the forebrain and face. Developmental Biology, 284(1), 48–61.

    CAS  PubMed  Google Scholar 

  • Marroig, 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(12), 2576–2600.

    CAS  PubMed  Google Scholar 

  • Martínez-Abadías, N., Esparza, M., Sjøvold, T., González-José, R., Santos, M., & Hernández, M. (2009). Heritability of human cranial dimensions: Comparing the evolvability of different cranial regions. Journal of Anatomy, 214, 19–35.

    PubMed  Google Scholar 

  • Mitteroecker, P. (2009). The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology. Evolutionary Biology. doi:10.1007/s11692-009-9075-6.

  • Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56(5), 818–836.

    PubMed  Google Scholar 

  • Monteiro, L. R., Bonato, V., & Dos Reis, S. F. (2005). Evolutionary integration and morphological diversification in complex morphological structures: Mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evolution & Development, 7(5), 429–439.

    Google Scholar 

  • Müller, G. B., & Newman, S. A. (2005). The innovation triad: An EvoDevo agenda. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 304(6), 487–503.

    PubMed  Google Scholar 

  • Muller, G. B., & Wagner, G. P. (1996). Homology, Hox genes, and developmental integration. American Zoologist, 36, 4–13.

    Google Scholar 

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

    Google Scholar 

  • Parsons, T. E., Kristensen, E., Hornung, L., Diewert, V. M., Boyd, S. K., German, R. Z., et al. (2008). Phenotypic variability and craniofacial dysmorphology: Increased shape variance in a mouse model for cleft lip. Journal of Anatomy, 212(2), 135–143.

    PubMed  Google Scholar 

  • Pavlicev, M., Cheverud, J., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.

    Google Scholar 

  • Petersson, S., Persson, A. S., Johansen, J. E., Ingvar, M., Nilsson, J., Klement, G., et al. (2003). Truncation of the Shaker-like voltage-gated potassium channel, Kv1.1, causes megencephaly. European Journal of Neuroscience, 18(12), 3231–3240.

    PubMed  Google Scholar 

  • Petersson, S., Sandberg Nordqvist, A., Schalling, M., & Lavebratt, C. (1999). The megencephaly mouse has disturbances in the insulin-like growth factor (IGF) system. Brain Research. Molecular Brain Research, 72(1), 80–88.

    CAS  PubMed  Google Scholar 

  • Porto, A., de Oliveira, F., Shirai, L., De Conto, V., & Marroig, G. (2009). The evolution of modularity in the mammalian skull I: Morphological integration patterns and magnitudes. Evolutionary Biology, 36(1), 118–135.

    Google Scholar 

  • Raff, R. A. (1996). The shape of life. Chicago: The University of Chicago Press.

    Google Scholar 

  • Raff, R. A., & Kaufman, T. C. (1983). Embryos, genes, and evolution. New York: MacMillan Publishers.

    Google Scholar 

  • Raff, R. A., & Sly, B. J. (2000). Modularity and dissociation in the evolution of gene expression territories in development. Evolution & Development, 2(2), 102–113.

    CAS  Google Scholar 

  • Richtsmeier, J. T., Aldridge, K., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., et al. (2006). Phenotypic integration of neurocranium and brain. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 306(4), 360–378.

    PubMed  Google Scholar 

  • Richtsmeier, J. T., & Deleon, V. B. (2009). Morphological integration of the skull in craniofacial anomalies. Orthodontics & Craniofacial Research, 12(3), 149–158.

    CAS  Google Scholar 

  • Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optical superimposition of landmarks. Systematic Zoology, 39(1), 40–59.

    Google Scholar 

  • Rolian, C. (2008). Developmental basis of limb length in rodents: Evidence for multiple divisions of labor in mechanisms of endochondral bone growth. Evolution & Development, 10(1), 15–28.

    Google Scholar 

  • Rolian, C. (2009). Integration and evolvability in primate hands and feet. Evolutionary Biology, 36(1), 100–117.

    Google Scholar 

  • Roseman, C., Kenny-Hunt, J., & Cheverud, J. (2009). Phenotypic integration without modularity: Testing hypotheses about the distribution of pleiotropic quantitative trait loci in a continuous space. Evolutionary Biology, 36(3), 282–291.

    Google Scholar 

  • Ruvinsky, I., & Gibson-Brown, J. J. (2000). Genetic and developmental bases of serial homology in vertebrate limb evolution. Development, 127(24), 5233–5244.

    CAS  PubMed  Google Scholar 

  • Savendahl, L. (2005). Hormonal regulation of growth plate cartilage. Hormone Research, 64(Suppl 2), 94–97.

    PubMed  Google Scholar 

  • Scharloo, W. (1964). Mutant expression and canalization. Nature, 203, 1095–1096.

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Schlosser, G., & Wagner, G. P. (2003). Introduction: The modularity concept in developmental and evolutionary biology. In G. Schlosser & G. P. Wagner (Eds.), Modularity in development and evolution (pp. 1–11). Chicago and London: The University of Chicago Press.

    Google Scholar 

  • Schmidt, M., & Fischer, M. S. (2009). Morphological integration in mammalian limb proportions: Dissociation between function and development. Evolution, 63(3), 749–766.

    PubMed  Google Scholar 

  • Sears, K. E., Behringer, R. R., Rasweiler, J. J., & Niswander, L. A. (2006). Development of bat flight: Morphologic and molecular evolution of bat wing digits. Proceedings of the National Academy of Sciences of the United States of America, 103(17), 6581–6586.

    CAS  PubMed  Google Scholar 

  • Steppan, S. J. (1997). Phylogenetic analysis of phenotypic covariance structure I. Contrasting results from matrix correlation and common principal component analysis. Evolution, 51, 571–586.

    Google Scholar 

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

    Google Scholar 

  • Wagner, G. P. (1989). A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Z. zool. Syst. Evolut. - forsch., 28, 48–61.

    Article  Google Scholar 

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

    Google Scholar 

  • Wagner, G. P. (2005). The developmental evolution of avian digit homology: An update. Theory in Biosciences, 124(2), 165–183.

    PubMed  Google Scholar 

  • Wagner, G. P., Booth, G., & Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution, 51(2), 329–347.

    Google Scholar 

  • Wagner, G. P., & Mezey, J. G. (2004). The role of genetic architecture constraints in the origin of variational modularity. In G. Schlosser & G. P. Wanger (Eds.), Modularity in development and evolution (pp. 338–358). Chicago and London: The University of Chicago Press.

    Google Scholar 

  • Wagner, G. P., Pavlicev, M., & Cheverud, J. (2007). The road to modularity. Nature Genetics, 8, 921–931.

    CAS  Google Scholar 

  • Wang, K.-Y., & Diewert, V. M. (1992). A morphometric analysis of craniofacial growth in cleft lip and noncleft mice. Journal of Craniofacial Genetics and Developmental Biology, 12(3), 141–154.

    CAS  PubMed  Google Scholar 

  • Willmore, K. E., Leamy, L., & Hallgrímsson, B. (2006). Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution and Development, 8(6), 550–567.

    PubMed  Google Scholar 

  • Willmore, K. E., Young, N. M., & Richtsmeier, J. T. (2007). Phenotypic variability: Its components, measurement and underlying developmental processes. Evolutionary Biology, 34(3–4), 99–120.

    Google Scholar 

  • Wright, S. (1932). General, group and special size factors. Genetics, 17, 603–619.

    CAS  PubMed  Google Scholar 

  • Young, N. M., Wagner, G. P., & Hallgrímsson, B. (submitted). Long legs and short arms: Development and evolvability of human limbs.

  • Young, N. M., & Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59(12), 2691–2704.

    PubMed  Google Scholar 

  • Young, N. M., Wat, S., Diewert, V. M., Browder, L. W., & Hallgrímsson, B. (2007). Comparative morphometrics of embryonic facial morphogenesis: Implications for cleft-lip etiology. The Anatomical Record (Hoboken), 290(1), 123–139.

    Google Scholar 

  • Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution & Development, 6(3), 194–206.

    Google Scholar 

  • Zelditch, M. L., Mezey, J., Sheets, H. D., Lundrigan, B. L., & Garland, T., Jr. (2006). Developmental regulation of skull morphology II: Ontogenetic dynamics of covariance. Evolution & Development, 8(1), 46–60.

    Google Scholar 

Download references

Acknowledgements

We are grateful to funding provided through National Science and Engineering Grant 238992-06, Canadian Foundation for Innovation grant #3923, Alberta Innovation and Science grant #URSI-01-103-RI, Canadian Institutes of Health Research grant #131625, Genome Canada and Genome Alberta grant to Hallgrímsson and NIH-NIDCR-R01DE018234 to Marcucio. We thank Wei Liu for computed microtomography scanning and landmarking and Mei Xiao for computer programming.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benedikt Hallgrímsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hallgrímsson, B., Jamniczky, H., Young, N.M. et al. Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation. Evol Biol 36, 355–376 (2009). https://doi.org/10.1007/s11692-009-9076-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-009-9076-5

Keywords

Navigation