Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation

Evolutionary Biology

Volumn 36, Issue 4, 2009, Pages 355-376

  Hallgrímsson, Benedikt ^a   Jamniczky, Heather ^a   Young, Nathan M ^a   Rolian, Campbell ^a   Parsons, Trish E ^a   Boughner, Julia C ^a   Marcucio, Ralph S ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Covariation; Developmental constraints; Evolvability; Mice; Morphological integration; Morphometrics; Primates; Rodents

Indexed keywords

MUS; PRIMATES; RODENTIA;

EID: 72249110894     PISSN: 00713260     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11692-009-9076-5     Document Type: Article

References (109)

1. 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.
2. Alberch, P. (1982). Developmental constraints in evolutionary processes. In J. T. Bonner (Ed.), Development in evolution (pp. 313-332). Berlin and New York: Springer.
3. 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.
4. 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.
5. Blechschmidt, I. E. (1961). The stages of human development before birth. An introduction to human embryology. Basel: Karger Medical Publishers.
6. Bookstein, F. L. (1991). Morphometric tools for landmark data. Cambridge: Cambridge University Press.
7. 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.
8. 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.
9. 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.
10. Burger, R. (1986). Evolutionary dynamics of functionally constrained phenotypic characters. IMA Journal of Mathematics Applied in Medicine and Biology, 3(4), 265-287.
11. Capdevila, J., & Izpisua Belmonte, J. C. (2001). Patterning mechanisms controlling vertebrate limb development. Annual Review of Cell and Developmental Biology, 17, 87-132.
12. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental integration in the cranium. Evolution, 36, 499-516.
13. Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155-171.
14. Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44-50.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40(1), 33-51.
28. Griswold, C. K. (2006). Pleiotropic mutation, modularity and evolvability. Evolution and Development, 8, 81-93.
29. Gunz, P., & Harvati, K. (2007). The Neanderthal "chignon": Variation, integration, and homology. Journal of Human Evolution, 52(3), 262-274.
30. Hagstrom, K. A., & Meyer, B. J. (2003). Condensin and cohesin: More than chromosome compactor and glue. Nature Reviews. Genetics, 4(7), 520-534.
31. Hall, B. K. (1999). Evolutionary developmental biology. Dordrecht: Kluwer.
32. 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.
33. 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.
34. Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48(3), 373-384.
35. 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.
36. 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.
37. 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.
38. Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology, 45, 131-158.
39. Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201-1219.
40. 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.
41. 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.
42. Hinchliffe, J. R., & Johnson, D. R. (1980). The development of the vertebrate limb. New York and London: Oxford University Press.
43. 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.
44. Hu, D., & Marcucio, R. S. (2009b). Unique organization of the frontonasal ectodermal zone in birds and mammals. Developmental Biology, 325(1), 200-210.
45. 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.
46. Jamniczky, H. A., & Hallgrímsson, B. (2009). A comparison of covariance structure in wild and laboratory muroid crania. Evolution, 63(6), 1540-1556.
47. 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.
48. 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.
49. 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.
50. 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.
51. Kember, N. F. (1993). Cell kinetics and the control of bone growth. Acta Paediatrica, 82(Suppl 391): 61-65.
52. Kirkwood, J., & Kember, N. (1993). Comparative quantitative histology of mammalian growth plates. Journal of Zoology, 231, 543-562.
53. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology and Systematics, 39, 115-132.
54. Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405-421.
55. Klingenberg, C. P., & Nijhout, H. F. (1999). Genetics of fluctuating asymmetry: A developmental model of developmental instability. Evolution, 53(2), 358-375.
56. 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.
57. 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.
58. Lieberman, D. E., McBratney, B. M., & Krovitz, G. (2002). The evolution and development of cranial form in Homo Sapiens. PNAS, 99(3), 1134-1139.
59. Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000). Basicranial influence on overall cranial shape. Journal of Human Evolution, 38(2), 291-315.
60. Love, A. (2006). Evolutionary morphology and Evo-devo: Hierarchy and novelty. Theory in Biosciences, 124(3), 317-333.
61. 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.
62. Magwene, P. M. (2001). New tools for studying integration and modularity. Evolution, 55(9), 1734-1745.
63. 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.
64. 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.
65. 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.
66. 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.
67. Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56(5), 818-836.
68. 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.
69. 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.
70. Muller, G. B., & Wagner, G. P. (1996). Homology, Hox genes, and developmental integration. American Zoologist, 36, 4-13.
71. Olson, E. C., & Miller, R. A. (1958). Morphological integration. Chicago: University of Chicago Press.
72. 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.
73. Pavlicev, M., Cheverud, J., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157-170.
74. 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.
75. 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.
76. 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.
77. Raff, R. A. (1996). The shape of life. Chicago: The University of Chicago Press.
78. Raff, R. A., & Kaufman, T. C. (1983). Embryos, genes, and evolution. New York: MacMillan Publishers.
79. 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.
80. 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.
81. Richtsmeier, J. T., & Deleon, V. B. (2009). Morphological integration of the skull in craniofacial anomalies. Orthodontics & Craniofacial Research, 12(3), 149-158.
82. Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optical superimposition of landmarks. Systematic Zoology, 39(1), 40-59.
83. 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.
84. Rolian, C. (2009). Integration and evolvability in primate hands and feet. Evolutionary Biology, 36(1), 100-117.
85. 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.
86. Ruvinsky, I., & Gibson-Brown, J. J. (2000). Genetic and developmental bases of serial homology in vertebrate limb evolution. Development, 127(24), 5233-5244.
87. Savendahl, L. (2005). Hormonal regulation of growth plate cartilage. Hormone Research, 64(Suppl 2), 94-97.
88. Scharloo, W. (1964). Mutant expression and canalization. Nature, 203, 1095-1096.
89. Scharloo, W. (1991). Canalization: Genetic and developmental aspects. Annual Review of Ecology and Systematics, 22, 65-93.
90. 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.
91. Schmidt, M., & Fischer, M. S. (2009). Morphological integration in mammalian limb proportions: Dissociation between function and development. Evolution, 63(3), 749-766.
92. 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.
93. 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.
94. Waddington, C. H. (1942). The canalisation of development and the inheritance of acquired characters. Nature, 150, 563.
95. Wagner, G. P. (1989). A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Z. zool. Syst. Evolut. - forsch., 28, 48-61.
96. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36-43.
97. Wagner, G. P. (2005). The developmental evolution of avian digit homology: An update. Theory in Biosciences, 124(2), 165-183.
98. Wagner, G. P., Booth, G., & Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution, 51(2), 329-347.
99. 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.
100. Wagner, G. P., Pavlicev, M., & Cheverud, J. (2007). The road to modularity. Nature Genetics, 8, 921-931.
101. 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.
102. 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.
103. 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.
104. Wright, S. (1932). General, group and special size factors. Genetics, 17, 603-619.
105. Young, N. M., Wagner, G. P., & Hallgrímsson, B. (submitted). Long legs and short arms: Development and evolvability of human limbs.
106. Young, N. M., & Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59(12), 2691-2704.
107. 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.
108. 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.
109. 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.