Skip to main content

Advertisement

SpringerLink
Log in

How to Explore Morphological Integration in Human Evolution and Development?

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

Abstract

Most studies in evolutionary developmental biology focus on large-scale evolutionary processes using experimental or molecular approaches, whereas evolutionary quantitative genetics provides mathematical models of the influence of heritable phenotypic variation on the short-term response to natural selection. Studies of morphological integration typically are situated in-between these two styles of explanation. They are based on the consilience of observed phenotypic covariances with qualitative developmental, functional, or evolutionary models. Here we review different forms of integration along with multiple other sources of phenotypic covariances, such as geometric and spatial dependencies among measurements. We discuss one multivariate method [partial least squares analysis (PLS)] to model phenotypic covariances and demonstrate how it can be applied to study developmental integration using two empirical examples. In the first example we use PLS to study integration between the cranial base and the face in human postnatal development. Because the data are longitudinal, we can model both cross-sectional integration and integration of growth itself, i.e., how cross-sectional variance and covariance is actually generated in the course of ontogeny. We find one factor of developmental integration (connecting facial size and the length of the anterior cranial base) that is highly canalized during postnatal development, leading to decreasing cross-sectional variance and covariance. A second factor (overall cranial length to height ratio) is less canalized and leads to increasing (co)variance. In a second example, we examine the evolutionary significance of these patterns by comparing cranial integration in humans to that in chimpanzees.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Armbruster, W. S., & Schwaegerle, K. E. (1996). Causes of covariation of phenotypic traits among populations. Journal of Evolutionary Biology, 9, 261–276.

    Article  Google Scholar 

  • Arnold, S. J., Bürger, R., Holenhole, P. A., Beverly, C. A., & Jones, A. G. (2008). Understanding the evolution and stability of the G-matrix. Evolution, 62, 2451–2461.

    Article  PubMed  Google Scholar 

  • Arnold, S. J., Pfrender, M. E., & Jones, A. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica, 112-113, 9–32.

    Article  PubMed  Google Scholar 

  • Arthur, W. (2002). The emerging conceptual framework of evolutionary developmental biology. Nature, 415(14), 757–764.

    Article  PubMed  CAS  Google Scholar 

  • Bastir, M., & Rosas, A. (2004). Facial heights: Evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. American Journal of Physical Anthropology, 47, 359–381.

    Google Scholar 

  • Bastir, M., & Rosas, A. (2005). Hierarchical nature of morphological integration and modularity in the human posterior face. American Journal of Physical Anthropology, 128(1), 26–34.

    Article  PubMed  Google Scholar 

  • Bastir, M., & Rosas, A. (2006). Correlated variation between the lateral basicranium and the face: A geometric morphometric study in different human groups. Archives of Oral Biology, 51, 814–824.

    Article  PubMed  Google Scholar 

  • Bastir, M., Rosas, A., Stringer, C., Manuel Cuétara, J., Kruszynski, R., Weber, G. W., et al. (2010). Effects of brain and facial size on basicranial form in human and primate evolution. Journal of Human Evolution, 58(5), 424–431.

  • Berg, R. L. (1960). The ecological significance of correlation pleiades. Evolution, 14, 171–180.

    Article  Google Scholar 

  • Bogin, B. (1999). Patterns of human growth. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bonner, J. T. (1988). The evolution of complexity by means of natural selection. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Bookstein, F. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Bookstein, F. (1996). Biometrics, biomathematics and the morphometric synthesis. Bulletin of Mathematical Biology, 58(2), 313–365.

    Article  PubMed  CAS  Google Scholar 

  • Bookstein, F. (1997). Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. Medical Image Analysis, 1(3), 225–243.

    Article  PubMed  CAS  Google Scholar 

  • Bookstein, F. L. (in press). Reasoning and measuring: Numerical inferences in the sciences. Cambridge: Cambridge University Press.

  • 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.

    Article  PubMed  Google Scholar 

  • Bulygina, E., Mitteroecker, P., & Aiello, L. C. (2006). Ontogeny of facial dimorphism and patterns of individual development within one human population. American Journal of Physical Anthropology, 131(3), 432–443.

    Google Scholar 

  • Chernoff, B., & Magwene, P. M. (1999). Morphological integration: Forty years later. In: Morphological integration, (pp. 319–354). Chicago: University of Chicago Press.

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42(5), 958–968.

    Article  Google Scholar 

  • Cheverud, J. M. (1989). A comparative analysis of morphological variation patterns in papionins. Evolution, 43, 1737–1747.

    Article  Google Scholar 

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

    Google Scholar 

  • Cheverud, J. M. (1996b). Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology, 9, 5–42.

    Article  Google Scholar 

  • Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989). Methods for the comparative analysis of variation patterns. Systematic Zoology, 38, 201–213.

    Article  Google Scholar 

  • Clausen, J., & Hiesey, W. M. (1960). The balance between coherence and variation in evolution. PNAS, 46(4), 494–506.

    Article  PubMed  CAS  Google Scholar 

  • Debat, V., & David, P. (2001). Mapping phenotypes: Canalization, plasticity and developmental stability. Trends in Ecology & Evolution, 16(10), 555–561.

    Article  Google Scholar 

  • Enlow, D., & Hans, M. (1996). Essentials of facial growth. Philadelphia, PA: Saunders Company.

    Google Scholar 

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

    Google Scholar 

  • Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Clarendon.

    Google Scholar 

  • Galis, F., Van Dooren, T. J., Feuth, J. D., Metz, J. A., Witkam, A., & Ruinard, S., et al. (2006). Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60(12), 2643–2654.

    PubMed  Google Scholar 

  • Gromko, M. H. (1995). Unpredictability of correlated response to selection: Pleiotropy and sampling interact. Evolution, 49, 685–693.

    Article  Google Scholar 

  • Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge: Harvard University Press.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In: D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Kluwer Press.

    Chapter  Google Scholar 

  • Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G. W., & Bookstein, F. L. (2009). Principles for the virtual reconstruction of hominin crania. Journal of Human Evolution, 57(1), 48–62.

    Article  PubMed  Google Scholar 

  • Haber, A. (2011). A Comparative Analysis of Integration Indices. Evolutionary Biology, 38, 476–488.

  • Hallgrimsson, B., Brown, J. J., 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.

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hallgrimsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parson, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355–376.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hallgrimsson, B., Lieberman, D. E., Young, N. M., Parsons, T., & Wat, S. (2007). Evolution of covariance in the mammalian skull. Novartis Found Symp 284 (Tinkering—The Microevolution of Development), 284, 164–190.

    Google Scholar 

  • Hansen, T. F. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems, 69(2–3), 83–94.

    Article  PubMed  Google Scholar 

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21(5), 1201–1219.

    Google Scholar 

  • Helms, J. A., Cordero, D., & Tapadia, M. D. (2005). New insights into craniofacial morphogenesis. Development, 132(5), 851–861.

    Google Scholar 

  • Hodgkin, J. (1998). Seven types of pleiotropy. The International Journal of Developmental Biology, 42(3), 501–505.

    PubMed  CAS  Google Scholar 

  • Houle, D. (1991). Genetic covariance of fitness correlates: What genetic correlations are made of and why it matters. Evolution, 45, 630–648.

    Article  Google Scholar 

  • Huttegger, S., & Mitteroecker, P. (2011). Invariance and meaningfulness in phenotype spaces. Evolutionary Biolog, 38, 335–352.

    Article  Google Scholar 

  • Huxley, J. S. (1932). Problems of relative growth. London: Methuen and Co.

    Google Scholar 

  • Klingenberg, C. P. (2008). Morphological Integration and Developmental Modularity. Annual Review of Ecology, Evolution and Systematics, 39, 115–132.

  • Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73, 70–123.

    Article  Google Scholar 

  • Klingenberg, C. P., Mebus, K., & Auffray, J. C. (2003). Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evolution & Development, 5(5), 522–531.

    Article  Google Scholar 

  • Klingenberg, C. P., & Zaklan, S. D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54(4), 1273–1285.

    PubMed  CAS  Google Scholar 

  • Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution, 33, 402–416.

    Article  Google Scholar 

  • Lande, R. (1980). The genetic covariance between characters maintained by pleiotropic mutations. Genetics, 94, 203–215.

    PubMed  CAS  Google Scholar 

  • Lande, R. (1984). The genetic correlation between characters maintained by selection, linkage and inbreeding. Genetical Research, 44, 309–320.

    Article  PubMed  CAS  Google Scholar 

  • Lieberman, D. E. (2011). The evolution of the human head. Cambridge, MA: Belknap Press/Harvard University Press.

    Google Scholar 

  • Lieberman, D. E., Ross, C., & Ravosa, M. J. (2000). The primate cranial base: Ontogeny, function, and integration. Yearbook of Physical Anthropology, 43, 117–169.

    Article  Google Scholar 

  • Leamy, L. (1977). Genetic and Environmental Correlations of Morphometric Traits in Randombred House Mice. Evolution, 31(2), 357–369.

    Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Marroig, G., & Cheverud, J. M. (2004). Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? American Naturalist, 163(3), 417–428.

    Google Scholar 

  • Martens, H., & Naes, T. (1989). Multivariate calibration. Chichester: Wiley.

    Google Scholar 

  • Martinez-Abadias, N., Esparza, M., Sjovold, T., Gonzalez-Jose, R., Santos, M., & Hernandez, M. (2009). Heritability of human cranial dimensions: Comparing the evolvability of different cranial regions. Journal of Anatomy, 214(1), 19–35.

    Article  PubMed  Google Scholar 

  • MartŠnez-AbadŠas, N., Esparza, M., Sj£vold, T., GonzĞlez-JosŐ, R., Santos, M., HernĞndez, M., et al. (in press). Pervasive genetic integration directs the evolution of human skull shape. Evolution.

  • Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., et al. (1985). Developmental constraints and evolution: A perspective from the mountain lake conference on development and evolution. The Quarterly Review of Biology, 60(3), 265–287.

    Article  Google Scholar 

  • Metscher, B. D. (2009). MicroCT for developmental biology: A versatile tool for high-contrast 3D imaging at histological resolutions. Developmental Dynamics, 238(3), 632–640.

    Google Scholar 

  • Metscher, B. D., & Müller, G. B. (2011). MicroCT for Molecular Imaging: Quantitative Visualization of Complete Three-Dimensional Distributions of Gene Products in Embryonic Limbs. Developmental Dynamics, 240, 2301–2308.

    Google Scholar 

  • Mitteroecker, P. (2009). The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology. Evolutionary Biology, 36, 377–385.

    Article  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. (2009). The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution, 63(3), 727–737.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. L. (2008). The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62(4), 943–958.

    Article  PubMed  Google Scholar 

  • Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Evolutionary Biology, 36, 235–247.

    Article  Google Scholar 

  • Mitteroecker, P., & Huttegger, S. (2009). The concept of morphospaces in evolutionary and developmental biology: Mathematics and metaphors. Biological Theory, 4(1), 54–67.

    Article  Google Scholar 

  • Monteiro, L. R., Bonato, V., & Reisb, 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.

    Article  Google Scholar 

  • Müller, G. B. (2003). Homology: The evolution of morphological organization. In: G. B. M§ller, & S. A. Newman (Eds.), Origination of organismal form: Beyond the gene in developmental and evolutionary biology. Cambridge, MA: MIT Press.

    Google Scholar 

  • Müller, G. B. (2007). Evo-devo: extending the evolutionary synthesis. Nature Reviews Genetics, 8(12), 943–949.

    Article  PubMed  Google Scholar 

  • Müller, G. B., & Newman, S. A. (1999). Generation, integration, autonomy: Three steps in the evolution of homology. Novartis Foundation Symposium, 222, 65–73.

    PubMed  Google Scholar 

  • Needham, J. (1933). On the dissociability of the fundamental processes in ontogenesis. Biological Reviews, 8, 180–223.

    Article  Google Scholar 

  • Neubauer, S., Gunz, P., & Hublin, J. -J. (2010). Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects. Journal of Human Evolution, 59, 555–566.

    Article  PubMed  Google Scholar 

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

  • Pavlicev, M., & Hansen, T. F. (2011). Genotype-phenotype maps maximizing evolvability: Modularity revisited. Evolutionary Biology, 38(4), 371–389.

    Article  Google Scholar 

  • Pavlicev, M., Wagner, G., & Cheverud, J. M. (2009). Measuring evolutionary constraints through the dimensionality of the phenotype: Adjusted bootstrap method to estimate rank of phenotypic covariance matrices. Evolutionary Biology, 36, 339–353.

    Article  Google Scholar 

  • Pigliucci, M. (2006). Genetic variance-covariance matrices: A critique of the evolutionary quantitative genetics research program. Biology and Philosophy, 21, 1–23.

    Article  Google Scholar 

  • Pigliucci, M., & Preston, K. (eds.) (2004). Phenotypic integration: Studying the ecology and evolution of complex phenotypes. Oxford: Oxford University Press.

    Google Scholar 

  • Raff, R. (1996). The shape of life: Genes, development, and the evolution of animal form. Chicago: Univeristy of Chicago Press.

    Google Scholar 

  • Riedl, R. J. (1978). Order in Living Organisms. New York: John Wiley and Sons.

  • Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman & Hall.

  • Rohlf, F. J., & Bookstein, F. (1987). A comment on shearing as a method for “size correction”. Systematic Zoology, 36, 356–367.

    Article  Google Scholar 

  • Rohlf, F. J., & Corti, M. (2000). The use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49, 740–753.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ross, C., & Henneberg, M. (1995). Basicranial flexion, relative brain size and facial kyphosis in Homo sapiens and some fossil hominids. American Journal of Physical Anthropology, 98, 575–593.

    Google Scholar 

  • Sawin, P. B., Fox, R. R., & Latimer, H. B. (1970). Morphogenetic studies of the rabbit XLI. Gradients of correlation in the architecture of morphology. American Journal of Anatomy, 128(2), 137–145.

    Article  PubMed  CAS  Google Scholar 

  • Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1174.

    Article  Google Scholar 

  • Sinervo, B., & Svensson, E. (2002). Correlational selection and the evolution of genomic architecture. Heredity, 89, 329–338.

    Article  PubMed  CAS  Google Scholar 

  • Sperber G. H. (2001). Craniofacial development. Ontario: BC Decker Inc..

  • Stadler, P. F., & Stadler, B. M. R. (2006). Genotype-phenotype maps. Biological Theory, 1(3), 268–279.

    Article  Google Scholar 

  • Tanner, J. M. (1963). Regulation of Growth in Size in Mammals. Nature, 199, 845–850.

    Google Scholar 

  • Terentjev, P. V. (1931). Biometrische Untersuchungen über die morphologischen Merkmale von Rana ridibunda Pall. (Amphibia, Salientia). Biometrika, 23, 23–51.

    Google Scholar 

  • Thompson, D. A. W. (1917). On growth and form. Cambridge: Cambridge University Press.

    Google Scholar 

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

    Article  Google Scholar 

  • Wagner, G., & Zhang, J. (2011). The pleiotropic structure of the genotype-phenotype map: The evolvability of complex organisms. Nature Reviews Genetics, 12, 204–213.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, G. P. (2000). What Is the Promise of Developmental Evolution? Part I: Why Is Developmental Biology Necessary to Explain Evolutionary Innovations? Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 288, 95–98.

    Article  CAS  Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967–976.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wright, S. (1932). General, group and special size factors. Genetics, 15, 603–619.

    Google Scholar 

  • Zelditch, M. L. (1987). Evaluating models of developmental integration in the laboratory rat using confirmatory factor analysis. Systematic Zoology, 36, 368–380.

    Article  Google Scholar 

  • Zelditch, M. L. (1988). Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution, 42(1), 28–41.

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgments

We thank Mihaela Pavlicev and Fred Bookstein for stimulating discussions and helpful comments on the manuscript. We are grateful to Ekaterina Stansfield for loaning us the digitized Denver growth study data.

Author information

Authors and Affiliations

  1. Department of Theoretical Biology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Philipp Mitteroecker & Gerd Müller

  2. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Philipp Gunz & Simon Neubauer

Authors
  1. Philipp Mitteroecker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philipp Gunz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simon Neubauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerd Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philipp Mitteroecker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mitteroecker, P., Gunz, P., Neubauer, S. et al. How to Explore Morphological Integration in Human Evolution and Development?. Evol Biol 39, 536–553 (2012). https://doi.org/10.1007/s11692-012-9178-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-012-9178-3

Keywords

Search

Navigation