Hostname: page-component-745bb68f8f-hvd4g Total loading time: 0 Render date: 2025-01-08T14:08:57.605Z Has data issue: false hasContentIssue false
  • English
  • Français

Methods for Studying Morphological Integration and Modularity

Published online by Cambridge University Press:  21 July 2017

Anjali Goswami  and
P. David Polly
Anjali Goswami
Affiliation:
Department of Genetics, Evolution and Environment and Department of Earth Sciences, University College London, Wolfson House 408, 4 Stephenson Way, London NW1 2HE UK
P. David Polly
Affiliation:
Department of Geological Sciences, Indiana University, 1001 E. 10th Street, Bloomington, IN 47401 USA
Get access

Abstract

Morphological integration and modularity are closely related concepts about how different traits of an organism are correlated. Integration is the overall pattern of intercorrelation; modularity is the partitioning of integration into evolutionarily or developmentally independent blocks of traits. Modularity and integration are usually studied using quantitative phenotypic data, which can be obtained either from extant or fossil organisms. Many methods are now available to study integration and modularity, all of which involve the analysis of patterns found in trait correlation or covariance matrices. We review matrix correlation, random skewers, fluctuating asymmetry, cluster analysis, Euclidean distance matrix analysis (EDMA), graphical modelling, two-block partial least squares, RV coefficients, and theoretical matrix modelling and discuss their similarities and differences. We also review different coefficients that are used to measure correlations. We apply all the methods to cranial landmark data from and ontogenetic series of Japanese macaques, Macaca fuscata to illustrate the methods and their individual strengths and weaknesses. We conclude that the exploratory approaches (cluster analyses of various sorts) were less informative and less consistent with one another than were the results of model testing or comparative approaches. Nevertheless, we found that competing models of modularity and integration are often similar enough that they are not statistically distinguishable; we expect, therefore, that several models will often be significantly correlated with observed data.

Type
Morphological Data
Information
The Paleontological Society Papers , Volume 16: Quantitative Methods in Paleobiology , October 2010 , pp. 213 - 243
Copyright
Copyright © 2010 by the Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdi, H. 2007. The RV coefficient and the congruence coefficient. In Salkind, N. (ed.), Encyclopedia of Measurement and Statistics. Sage, Thousand Oaks, CA.Google Scholar
Ackermann, R. R., and Cheverud, J. M. 2000. Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal components analysis. American Journal of Physical Anthropology, 111:489–501.3.0.CO;2-U>CrossRefGoogle Scholar
Ackermann, R. R., and Cheverud, J. M. 2004a. Morphological integration in primate evolution., p. 302–319. In Pigliucci, M. and Preston, K. (eds.), Phenotypic Integration. Oxford University Press, Oxford.CrossRefGoogle Scholar
Ackermann, R. R., and Cheverud, J. M. 2004b. Detecting genetic drift versus selection in human evolution. Proceedings of the National Academy of Sciences USA, 101: 17946–17951.CrossRefGoogle ScholarPubMed
Arnold, S. 1992. Constraints on phenotypic evolution. American Naturalist, 140:S85.CrossRefGoogle ScholarPubMed
Arnold, S., Burger, R., Hohenlohe, P., Ajie, B., and Jones, A. 2008. Understanding the evolution and stability of the G-matrix. Evolution, 62:2451–2461.CrossRefGoogle ScholarPubMed
Atchley, W. R. 1993. Genetic and developmental aspects of variability in the mammalian mandible, p. 207–247. In Hanken, J. and Hall, B. K. (eds.), The Skull. Volume 1. Development. University of Chicago Press, Chicago.Google Scholar
Atchley, W. R., and Hall, B. K. 1991. A model for development and evolution of complex morphological structures. Biological Reviews, 66:101–157.CrossRefGoogle Scholar
Atchley, W. R., Rutledge, J. J., and Cowley, D. E. 1982. A multivariate statistical analysis of direct and correlated response to selection in the rat. Evolution, 36:677–698.CrossRefGoogle Scholar
Badyaev, A. V., and Foresman, K. R. 2000. Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proceedings of the Royal Society of London Biological Sciences, Series B, 267:371–377.CrossRefGoogle ScholarPubMed
Badyaev, A. V., and Martin, T. E. 2000. Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus). Journal of Evolutionary Biology; 13:290–301.CrossRefGoogle Scholar
Badyaev, A. V., and Foresman, K. R. 2004. Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. American Naturalist, 163:868–879.CrossRefGoogle ScholarPubMed
Badyaev, A. V., Foresman, K. R., and Young, R. L. 2005. Evolution of morphological integration: developmental accomodation of stress-induced variation. American Naturalist, 166:382–395.CrossRefGoogle Scholar
Bastir, M., and Rosas, A. 2005. The hierarchical nature of morphological integration and modularity in the human posterior face. American Journal of Physical Anthropology, 128:26–34.CrossRefGoogle ScholarPubMed
Bastir, M., and 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.CrossRefGoogle Scholar
Bennett, C. V., and Goswami, A. in press. Does reproductive strategy drive limb integration in marsupials and monotremes? Mammalian Biology.Google Scholar
Bolker, J. A. 2000. Modularity in development and why it matters to evo-devo. American Zoologist, 40:770–776.Google Scholar
Bookstein, F. L. 1991. Morphometric Tools for Landmark Data. Cambridge University Press, Cambridge, 435 p.Google Scholar
Bookstein, F. L., Gunz, P., Mitteroecker, P., Prossinger, H., Schaefer, K., and Seidler, H. 2003. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. Journal of Human Evolution, 44:167–187.CrossRefGoogle ScholarPubMed
Boughner, J., Wat, S., Diewert, V., Young, N., Browder, L., and Hallgrímsson, B. 2008. Short-faced mice and developmental interactions between the brain and the face. Journal of Anatomy, 213:646–662.CrossRefGoogle ScholarPubMed
Bruner, E. 2008. Comparing Endocranial Form and Shape Differences in Modern Humans and Neandertals: a Geometric Approach. PaleoAnthropology, 2008:93–106.Google Scholar
Bruner, E., and Ripani, M. 2008. A quantitative and descriptive approach to morphological variation of the endocranial base in modern humans. American Journal of Physical Anthropology, 137:30–40.CrossRefGoogle ScholarPubMed
Burt, C. 1948. Factor analysis and canonical correlations. British Journal of Psychology, 1:95–106.Google Scholar
Chapman, R. E. 1990. Conventional Procrustes approaches, p. 251–267. In Rohlf, F. J. and Bookstein, F. L. (eds.), Proceedings of the Michigan Morphometrics Workshop. University of Michigan Museum of Zoology, Ann Arbor, Michigan.Google Scholar
Chernoff, B., and Magwene, P. M. 1999. Afterword, p. 319–348, In Olson, E. C. and Miller, R. L., Morphological Integration. University of Chicago Press, Chicago.Google Scholar
Cheverud, J. M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36:499–516.CrossRefGoogle ScholarPubMed
Cheverud, J. M. 1988. A comparison of genetic and phenotypic correlations. Evolution, 42:958–968.CrossRefGoogle ScholarPubMed
Cheverud, J. M. 1988. Spatial-analysis in morphology illustrated by rhesus macaque cranial growth and integration. American Journal of Physical Anthropology, 75:195–196.Google Scholar
Cheverud, J. M. 1989. A comparative analysis of morphological variation patterns in the Papionines. Evolution, 43:1737–1747.CrossRefGoogle Scholar
Cheverud, J. M. 1995. Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145:63–89.CrossRefGoogle Scholar
Cheverud, J. M. 1996a. Developmental integration and the evolution of pleiotropy. American Zoologist, 36:44–50.CrossRefGoogle 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.CrossRefGoogle Scholar
Cheverud, J. M. 2004. Modular pleiotropic effects of quantitative trait loci on morphological traits, p. 132–153. In Schlosser, G. and Wagner, G. P. (eds.), Modularity in development and evolution. University of Chicago, Chicago.Google Scholar
Cheverud, J. M., Rutledge, J. J., and Atchley, W. R. 1983. Quantitative genetics of development: Genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution, 37:895–905.Google ScholarPubMed
Cheverud, J. M., Wagner, G. P., and Dow, M. M. 1989. Methods for the comparative analysis of variation patterns. Systematic Zoology, 38:201–213.CrossRefGoogle Scholar
Cheverud, J. M., Routman, E. J., and Irschick, D. J. 1997. Pleiotropic effects of individual gene loci on mandibular morphology. Evolution, 51:2006–2016.CrossRefGoogle ScholarPubMed
Cheverud, J. M., Hartman, S. E., Richtsmeier, J. T., and Atchley, W. R. 1991. A quantitative genetic-analysis of localized morphology in mandibles of inbred mice using finite-element scaling analysis. Journal of Craniofacial Genetics and Developmental Biology, 11:122–137.Google ScholarPubMed
Cheverud, J. M., Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., and Pletscher, L. S. 2004. Pleiotropic effects on mandibular morphology II: Differential epistasis and genetic variation in morphological integration. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 302B:424–435.CrossRefGoogle Scholar
Cole, T.M. III, and Richtsmeier, J. 1998. A simple method for visualization of influential landmarks when using Euclidean distance matrix analysis. American Journal of Physical Anthropology, 107:273–283.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Conner, J. 2002. Genetic mechanisms of floral trait correlations in a natural population. Nature, 420:407–410.CrossRefGoogle Scholar
de Oliveira, F. B., Porto, A., and Marroig, G. 2009. Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution. Journal of Human Evolution, 56:417–430.CrossRefGoogle ScholarPubMed
de Visser, J., Hermisson, J., Wagner, G. P., Meyers, L., Bagheri-Chaichian, H., Blanchard, J., Chao, L., Cheverud, J. M., Elena, S., and Fontana, W. 2003. Perspective: evolution and detection of genetic robustness. Evolution, 57:1959–1972.Google ScholarPubMed
Draghi, J., and Wagner, G. P. 2007. Evolution of evolvability in a developmental model. Evolution, 62:301–315.CrossRefGoogle Scholar
Drake, A. G., and Klingenberg, C. P. 2010. Large-scale diversification of skull shape in domestic dogs: disparity and modularity. American Naturalist, 175:289–301.CrossRefGoogle ScholarPubMed
Dryden, I. L., and Mardia, K. V. 1998. Statistical Shape Analysis. John Wiley & Sons, Chichester, U.K. 347 p.Google Scholar
Eble, G. 2004. The macroevolution of phenotypic integration, p. 253–273. In Pigliucci, M. and Preston, K. (eds.), Phenotypic Integration. Oxford University Press, Oxford.CrossRefGoogle Scholar
Ehrich, T. H., Vaughn, T. T., Koreishi, S., Linsey, R. B., Pletscher, L. S., and Cheverud, J. M. 2003. Pleiotropic effects on mandibular morphology I. Developmental morphological integration and differential dominance. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 296B:58–79.CrossRefGoogle Scholar
Emerson, S. B., and Hastings, P. A. 1998. Morphological correlations in evolution: Consequences for phylogenetic analysis. The Quarterly Review of Biology, 73:141–162.CrossRefGoogle Scholar
Escoufier, Y. 1973. Le traitement des variables vectorielles. Biometrics, 29:751–760.CrossRefGoogle Scholar
Fink, W. L., and Zelditch, M. L. 1996. Historical patterns of developmental integration in Pirhanas. American Zoologist, 36:61–69.CrossRefGoogle Scholar
Gonzalez-Jose, R., Escapa, I., Neves, W., Cuneo, R., and Pucciarelli, H. 2008. Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature, 453:775–778.CrossRefGoogle ScholarPubMed
Goswami, A. 2006a. Cranial modularity shifts during mammalian evolution. American Naturalist, 168:270–280.CrossRefGoogle ScholarPubMed
Goswami, A. 2006b. Morphological integration in the carnivoran skull. Evolution, 60:169–183.Google ScholarPubMed
Goswami, A. 2007a. Cranial integration, phylogeny, and diet in australodelphian marsupials. PLoSOne, 2:e995.CrossRefGoogle ScholarPubMed
Goswami, A. 2007b. Cranial modularity and sequence heterochrony in mammals. Evolution & Development, 9:290–298.CrossRefGoogle ScholarPubMed
Goswami, A., and Polly, P. D. 2010a. The influence of character correlations of phylogenetic analyses: a case study of the carnivoran cranium, p. 141–164. In Goswami, A. and Friscia, A. (eds.), Carnivoran Evolution: New Views on Phylogeny, Form, and Function. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Goswami, A., and Polly, P. D. 2010b. The influence of modularity on cranial morphological diversity in Carnivora and Primates (Mammalia; Placentalia). PLoS One, 5:e9517.CrossRefGoogle Scholar
Goswami, A., Weisbecker, V., and Sánchez-Villagra, M. R. 2009. Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Zoology, 312B:186–195.CrossRefGoogle ScholarPubMed
Hallgrímsson, B., Willmore, K., and Hall, B. 2002. Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology, 119:131–158.CrossRefGoogle Scholar
Hallgrímsson, B., Dorval, C., Zelditch, M., and German, R. 2004a. Craniofacial variability and morphological integration in mice susceptible to cleft lip and palate. Journal of Anatomy, 205:501.CrossRefGoogle ScholarPubMed
Hallgrímsson, B., Willmore, K., Dorval, C., and Cooper, D. M. L. 2004b. Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 302B:207–225.CrossRefGoogle Scholar
Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., and Marcucio, R. S. in press. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology.Google Scholar
Hansen, T., and Houle, D. 2008. Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21:1201–1219.CrossRefGoogle ScholarPubMed
Hermisson, J., and Wagner, G. P. 2004. Evolution of phenotypic robustness, p. 47–70. In Jen, E. (ed.), Robust Design: A Repertoire from Biology, Ecology, and Engineering Case Studies. Oxford University Press, Oxford.Google Scholar
HOTELLING, H. 1936. Relations between two sets of variates. Biometrika, 28:321.CrossRefGoogle Scholar
Jolicoeur, P., and Mosimann, J. E. 1960. Size and shape variation in the painted turtle. A principal component analysis. Growth, 24:339–354.Google Scholar
Jollife, I. T. 2002. Principal Components Analysis. Springer-Verlag, New York, 487 p.Google Scholar
Jones, A., Arnold, S., and Bürger, R. 2007. The mutation matrix and the evolution of evolvability. Evolution, 61:727–745.CrossRefGoogle ScholarPubMed
Klingenberg, C. P. 2003. Developmental instability as a research tool: using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. Developmental instability: causes and consequences:427–442.CrossRefGoogle Scholar
Klingenberg, C. P. 2004. Integration, modules, and development: molecules to morphology to evolution, p. 213–230. In Pigliucci, M. and Preston, K. (eds.), Phenotypic Integration. Oxford University Press, Oxford.CrossRefGoogle Scholar
Klingenberg, C. P. 2005. Developmental constraints, modules, and evolvability, p. 219–247. In Hallgrimsson, B. and Hall, B. K. (eds.), Variation. Academic Press, San Diego.CrossRefGoogle Scholar
Klingenberg, C. P. 2008a. Morphological integration and developmental modularity. Annual Review of Ecology, Evolution and Systematics, 39: 115–132.CrossRefGoogle Scholar
Klingenberg, C. P. 2008b. MorphoJ. http://www.flywings.org.uk/MorphoJ_page.htm. Faculty of Life Sciences, University of Manchester, UK.Google Scholar
Klingenberg, C. P. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evolution & Development, 11:405–421.CrossRefGoogle ScholarPubMed
Klingenberg, C. P., and Zaklan, S. D. 2000. Morphological integration between developmental compartments in the Drosophila wing. Evolution, 53:358–375.CrossRefGoogle Scholar
Klingenberg, C. P., and Leamy, L. J. 2001. Quantitative genetics of geometric shape in the mouse mandible. Evolution, 55:2342–2352.Google ScholarPubMed
Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., and Beckwith, N. J. 2001a. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. American Naturalist, 157:11–23.CrossRefGoogle ScholarPubMed
Klingenberg, C. P., Leamy, L. J., Routman, E. J., and Cheverud, J. M. 2001b. Genetic architecture of mandible shape in mice: Effects of quantitative trait loci analyzed by geometric morphometrics. Genetics, 157:785–802.CrossRefGoogle ScholarPubMed
Klingenberg, C., Barluenga, M., and Meyer, A. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution, 56:1909–1920.Google ScholarPubMed
Klingenberg, C. P., Mebus, K., and Auffray, J. C. 2003. Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evolution & Development, 5:522–531.CrossRefGoogle Scholar
Klingenberg, C. P., Leamy, L. J., and Cheverud, J. M. 2004. Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics, 166:1909–1921.CrossRefGoogle ScholarPubMed
Lauritzen, S. L. 1996. Graphical Models. Clarendon Press, Oxford, x, 298 p.CrossRefGoogle Scholar
Leamy, L. J., Routman, E. J., and Cheverud, J. M. 1999. Quantitative trait loci for early- and late-developing skull characters in mice: A test of the genetic independence model of morphological integration. American Naturalist, 153:201–214.CrossRefGoogle ScholarPubMed
Leamy, L. J., Routman, E. J., and Cheverud, J. M. 2002. An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution, 56:642–653.Google ScholarPubMed
Legendre, P., and Legendre, L. 1998. Numerical Ecology, Elsevier Science, Amsterdam, 870 p.Google Scholar
Lele, S., and Richtsmeier, J. 1991. Euclidean distance matrix analysis: a coordinate-free approach for comparing biological shapes using landmark data. American Journal of Physical Anthropology, 86:415–427.CrossRefGoogle ScholarPubMed
Lele, S., and Richtsmeier, J. 2001. An Invariant Approach to Statistical Analysis of Shapes. CRC Press, Boca Raton, FL, 308 p.CrossRefGoogle Scholar
Lele, S. R. 1999. Invariance and morphometrics: a critical appraisal of statistical techniques for landmark data, p. 325–336. In Chaplain, M., Singh, G., and McLachlan, J. (eds.), On Growth and Form: Spatiotemporal Pattern Formation in Biology. John Wiley and Sons, Chichester, UK.Google Scholar
Lieberman, D. E., Ross, C. F., and Ravosa, M. J. 2000a. The primate cranial base: Ontogeny, function, and integration. Yearbook of Physical Anthropology, 43:117–169.3.0.CO;2-I>CrossRefGoogle Scholar
Lieberman, D. E., Pearson, O. M., and Mowbray, K. M. 2000b. Basicranial influence on overall cranial shape. Journal of Human Evolution, 38:291–315.CrossRefGoogle ScholarPubMed
Magwene, P. M. 2001. New tools for studying integration and modularity. Evolution, 55:1734–1745.Google ScholarPubMed
Magwene, P. M. 2008. Using correlation proximity graphs to study phenotypic integration. Evolutionary Biology, 35:191–198.CrossRefGoogle Scholar
Magwene, P. M. 2009. Statistical methods for studying modularity: A reply to Mitteroecker and Bookstein. Systematic Biology, 58:146–149.CrossRefGoogle ScholarPubMed
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research, 27:209–220.Google Scholar
Márquez, E. J. 2008. A statistical framework for testing modularity in multidimensional data. Evolution, 62:2688–2708.CrossRefGoogle ScholarPubMed
Marroig, G., and 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 ScholarPubMed
Marroig, G., and Cheverud, J. M. 2004. Cranial evolution in sakis (Pithecia, platyrrhini) I: Interspecific differentiation and allometric patterns. American Journal of Physical Anthropology, 125:266–278.CrossRefGoogle ScholarPubMed
Marroig, G., and Cheverud, J. 2005. Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in new world monkeys. Evolution, 59:1128–1142.Google ScholarPubMed
Marroig, G., Vivo, M., and Cheverud, J. M. 2004. Cranial evolution in sakis (Pithecia, Platyrrhini) II: Evolutionary processes and morphological integration. Journal of Evolutionary Biology, 17:144–155.CrossRefGoogle ScholarPubMed
McGuigan, K., Chenoweth, S., and Blows, M. 2005. Phenotypic divergence along lines of genetic variance. American Naturalist, 165:32–43.CrossRefGoogle ScholarPubMed
Mitteroecker, P., and Bookstein, F. 2007. The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56:818–836.CrossRefGoogle ScholarPubMed
Mitteroecker, P., and Bookstein, F. 2009. Examining modularity via partial correlations: a rejoinder to a comment by Paul Magwene. Systematic Biology, 58:346–348.CrossRefGoogle ScholarPubMed
Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., and Bookstein, F. L. 2004. Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46:679–697.CrossRefGoogle ScholarPubMed
Monteiro, L., Bonato, V., and dos Reis, S. 2005. Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evolution & Development, 7:429–439.CrossRefGoogle ScholarPubMed
Moss, M. O., and Young, R. W. 1960. A functional approach to craniology. American Journal of Physical Anthropology, 18:281–291.CrossRefGoogle ScholarPubMed
Nijhout, H. 2002. The nature of robustness in development. BioEssays, 24:553–563.CrossRefGoogle ScholarPubMed
O'Keefe, F. R., and Wagner, P. J. 2001. Inferring and testing hypotheses of cladistic character dependence by using character compatibility. Systematic Biology, 50:657–675.CrossRefGoogle ScholarPubMed
Olson, E. C., and Miller, R. L. 1958. Morphological Integration. University of Chicago Press, Chicago, 376 p.Google Scholar
Palmer, A., and Strobeck, C. 1986. Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17:391–421.CrossRefGoogle Scholar
Pavlicev, M., Cheverud, J. M., and Wagner, G. P. 2009. Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36:157–170.CrossRefGoogle Scholar
Phillips, P. C., and Arnold, S. J. 1999. Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution, 53:1506–1515.Google ScholarPubMed
Pielou, E. C. 1984. Probing multivariate data with random skewers: a preliminary to direct gradient analysis. Oikos, 42:161–165.CrossRefGoogle Scholar
Pigliucci, M., and Preston, K. 2004. Phenotypic Integration. Oxford University Press, Oxford, 464 p.CrossRefGoogle Scholar
Polly, P. D. 2001. On morphological clocks and paleophylogeography: towards a timescale for Sorex hybrid zones. Genetica, 112:339–357.CrossRefGoogle ScholarPubMed
Polly, P. D. 2004. On the simulation of morphological shape: mutivariate shape under selection and drift, Palaeontologia Electronica, 7:7A.Google Scholar
Polly, P. D. 2005. Development and phenotypic correlations: the evolution of tooth shape in Sorex araneus. Evolution & Development, 7:29–41.CrossRefGoogle ScholarPubMed
Polly, P. D. 2008. Developmental dynamics and G-matrices: Can morphometric spaces be used to model phenotypic evolution? Evolutionary Biology, 35:83–96.CrossRefGoogle Scholar
Raup, D. 1975. Taxonomic diversity estimation using rarefaction. Paleobiology:333–342.CrossRefGoogle Scholar
Renaud, S., Auffray, J., and Michaux, J. 2006. Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Evolution: 1701–1717.Google Scholar
Rice, S. 1998. The evolution of canalization and the breaking of Von Baer's laws: Modeling the evolution of development with epistasis. Evolution, 52:647–656.CrossRefGoogle ScholarPubMed
Rice, S. H. 2008. The G-matrix as one piece of the phenotypic evolution puzzle. Evolutionary Biology, 35:106–107.CrossRefGoogle Scholar
Richtsmeier, J., and Lele, S. 1993. A coordinate-free approach to the analysis of growth patterns: models and theoretical considerations. Biological Reviews, 68:381–381.CrossRefGoogle Scholar
Richtsmeier, J. T., DeLeon, V. B., and Lele, S. R. 2002. The promise of geometric morphometrics. American Journal of Physical Anthropology, 119 (S35):63–91.CrossRefGoogle Scholar
Roff, D. 1995. The estimation of genetic correlations from phenotypic correlations: a test of Cheverud's conjecture. Heredity, 74:481–490.CrossRefGoogle Scholar
Roff, D. 2000. The evolution of the G matrix: selection or drift? Heredity, 84:135–142.CrossRefGoogle ScholarPubMed
Roff, D., and Mousseau, T. 2005. The evolution of the phenotypic covariance matrix: evidence for selection and drift in Melanoplus. Journal of Evolutionary Biology, 18:1104–1114.CrossRefGoogle ScholarPubMed
Rohlf, F. J. 1990. Rotational fit Procrustes methods. University of Michigan Museum of Zoology Special Publications, 2:227–236.Google Scholar
Rohlf, F. J. 1993. Relative warp analysis and an example of its application to mosquito wings., p. 131–159. In Marcus, L. F., Bello, E., and Garcia-Valdecasas, A. (eds.), Contributions to Morphometrics. Museo National de Ciencias Naturales, Madrid.Google Scholar
Rohlf, F. J. 2000. On the use of shape spaces to compare morphometric methods. Hystrix, 11:9–25.Google Scholar
Rohlf, F. J. 2003. Bias and error in estimates of mean shape in geometric morphometrics. Journal of Human Evolution, 44:665–683.CrossRefGoogle ScholarPubMed
Rohlf, F. J., and Slice, D. 1990. Extentions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39:40–59.CrossRefGoogle Scholar
Rohlf, F. J., and Corti, M. 2000. Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49:740–753.CrossRefGoogle ScholarPubMed
Sadleir, R. W., and Makovicky, P. J. 2008. Cranial shape and correlated characters in crocodile evolution. Journal of Evolutionary Biology, 21:1578–1596.CrossRefGoogle ScholarPubMed
Sanders, H. 1968. Marine benthic diversity: a comparative study. American Naturalist, 102:243.CrossRefGoogle Scholar
Schlosser, G., and Wagner, G. P. 2004. Modularity in development and evolution. University of Chicago Press, Chicago, 600 p.Google Scholar
Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution, 50:1766–1774.CrossRefGoogle ScholarPubMed
Schwenk, K. 2001. Functional units and their evolution, p. 165–198. In Wagner, G. P. (ed.), The character concept in evolutionary biology. Academic Press, San Diego, CA.CrossRefGoogle Scholar
Sneath, P., and Sokal, R. 1973. Numerical Taxonomy: the Principles and Practice of Numerical Classification. W.H. Freeman, San Francisco, 588 p.Google Scholar
Steppan, S. 1997. Phylogenetic analysis of phenotypic covariance structure. I. Contrasting results from matrix correlation and common principal component analysis. Evolution, 51:571–586.Google Scholar
Steppan, S., Phillips, P., and Houle, D. 2002. Comparative quantitative genetics: evolution of the G matrix. Trends in Ecology & Evolution, 17:320–327.CrossRefGoogle Scholar
Strait, D. S. 2001. Integration, phytogeny, and the hominid cranial base. American Journal of Physical Anthropology 114:273–297.CrossRefGoogle Scholar
Streissguth, A., Bookstein, F., Sampson, P., and Barr, H. 1993. The enduring effects of prenatal alcohol exposure on child development: Birth through seven years, a partial least squares solution. University of Michigan Press, Ann Arbor.Google Scholar
van der Klaauw, C. J. 1948–1952. Size and position of the functional components of the skull. Archives Neerlandaises de Zoologie, 9:1–559.CrossRefGoogle Scholar
Van Valen, L. 1962. A study of fluctuating asymmetry. Evolution, 16:125–142.CrossRefGoogle Scholar
Vermeij, G. J. 1973. Adaptation, versatility, and evolution. Systematic Zoology, 22:466–477.CrossRefGoogle Scholar
Waddington, C. 1942. Canalization of development and the inheritance of acquired characters. Nature, 150:563–565.CrossRefGoogle Scholar
Wagner, A. 2008. Robustness and evolvability: a paradox resolved. Proceedings of the Royal Society of London, Series B, 275:91.Google ScholarPubMed
Wagner, G. P. 1988. The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution. Journal of Evolutionary Biology, 1:45–66.CrossRefGoogle Scholar
Wagner, G. P. 1995. Adaptation and the modular design of organisms. Advances in Artificial Life, 929:317–328.Google Scholar
Wagner, G. P. 1996. Homologues, natural kinds and the evolution of modularity. American Zoologist, 36:36–43.CrossRefGoogle Scholar
Wagner, G. P., and Altenberg, L. 1996. Perspective: Complex adaptations and the evolution of evolvability. Evolution, 50:967–976.CrossRefGoogle ScholarPubMed
Wagner, G. P., and Mezey, J. G. 2004. The role of genetic architecture contraints in the origin of variational modularity, p. 338–358. In Schlosser, G. and Wagner, G. P. (eds.), Modularity in Development and Evolution. University of Chicago Press, Chicago.Google Scholar
Wagner, G. P., Booth, G., and Bagheri-Chaichian, H. 1997. A population genetic theory of canalization. Evolution, 51:329–347.CrossRefGoogle ScholarPubMed
Wagner, G. P., Pavlicev, M., and Cheverud, J. M. 2007. The road to modularity. Nature Genetics, 8:921–931.CrossRefGoogle ScholarPubMed
Wagner, P. J. 1998. A likelihood approach for evaluating estimates of phylogenetic relationships among fossil taxa. Paleobiology, 24:430–449.CrossRefGoogle Scholar
Ward, J. Jr 1963. Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58:236–244.CrossRefGoogle Scholar
Webster, M., and Zelditch, M. L. 2008. Integration and regulation of developmental systems in trilobites. Cuadernos del Museo Geominero, 9:427–433.Google Scholar
Whittaker, J. 1990. Graphical Models in Applied Multivariate Statistics. Wiley, Chichester U.K., 448 p.Google Scholar
Young, N., and Hallgrímsson, B. 2005. Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59:2691–2704.Google ScholarPubMed
Zelditch, M. L. 1988. Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution, 42:28–41.CrossRefGoogle ScholarPubMed
Zelditch, M. L., and Carmichael, A. C. 1989a. Growth and intensity of integration through postnatal growth in the skull of Sigmodon fulviventer . Journal of Mammalogy, 70:477–484.CrossRefGoogle Scholar
Zelditch, M. L., and Carmichael, A. C. 1989b. Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fuliviventer . Evolution 43:814–824.CrossRefGoogle Scholar
Zelditch, M. L., and Moscarella, R. A. 2004. Form, function and life history: spatial and temporal dynamics of integration, p. 274–301 In Pigliucci, M. and Preston, K. (eds.), Phenotypic Integration. Oxford University Press, Oxford.CrossRefGoogle Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2001. The spatial complexity and evolutionary dynamics of growth, p. 145–194 In Zelditch, M. L. (ed.), Beyond Heterochrony: the Evolution of Development. Wiley-Liss, Inc., New York.Google Scholar
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., and Fink, W. L. 2004. Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, San Diego, 416 p.Google Scholar
Zelditch, M. L., Mezey, J., Sheets, H., Lundrigan, B., and Garland, T. 2006. Developmental regulation of skull morphology II: Ontogenetic dynamics of covariance. Evolution and Development, 8:46–60.CrossRefGoogle ScholarPubMed
Zelditch, M. L., Wood, A. R., Bonett, R. M., and Swiderski, D. L. 2008. Modularity of the rodent mandible: Integrating bones, muscles, and teeth. Evolution & Development, 10:756–768.CrossRefGoogle ScholarPubMed
Zelditch, M. L., Wood, A., and Swiderski, D. 2009. Building developmental integration into functional systems: function-induced integration of mandibular shape. Evolutionary Biology, 36:71–87.CrossRefGoogle Scholar