Building developmental integration into functional systems: Function-induced integration of mandibular shape

Evolutionary Biology

Volumn 36, Issue 1, 2009, Pages 71-87

  Zelditch, Miriam Leah ^a   Wood, Aaron R ^a   Swiderski, Donald L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Mandible; Modularity; Morphological integration

Indexed keywords

MAMMALIA; PEROMYSCUS; PEROMYSCUS MANICULATUS BAIRDII; RODENTIA; SCIURIDAE; SCIURUS NIGER;

EID: 69849091106     PISSN: 00713260     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11692-008-9034-7     Document Type: Article

References (83)

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. doi:10.1002/(SICI)1096-8644(200004)111:4<489::AID-AJPA5>3.0.CO;2-U.
2. Ackermann, R. R., & Cheverud, J. M. (2004). Morphological integration in primate evolution. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 302-319). Oxford: Oxford University Press.
3. Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the 'revolution'. The Italian Journal of Zoology, 71(1), 5-16.
4. Allen, C. E. (2008). The "Eyespot Module" and eyespots as modules: Development, evolution, and integration of a complex phenotype. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 310B(2), 179-190. doi:10.1002/jez.b.21186.
5. Andresen, P. R., Bookstein, F. L., Conradsen, K., Ersbøll, B., Marsh, J., & Kreiborg, S. (2000). Surface-bounded growth modeling applied to human mandibles. IEEE Transactions on Medical Imaging, 19, 1053-1063. doi:10.1109/42.896780.
6. Armbruster, W. S., Di Stilio, V. S., Tuxill, J. D., Flores, T. C., & Runk, J. L. V. (1999). Covariance and decoupling of floral and vegetative traits in nine neotropical plants: A re-evaluation of Berg's correlation pleiades concept. American Journal of Botany, 86(1), 39-55. doi:10.2307/2656953.
7. Atchley, W. R. (1993). Genetic and developmental aspects of variability in the mammalian mandible. In J. Hanken & B. K. Hall (Eds.), The Skull (pp. 207-247). Chicago: University of Chicago Press.
8. Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews of the Cambridge Philosophical Society, 66(2), 101-157. doi:10.1111/j.1469-185X.1991.tb01138.x.
9. Atchley, W. R., Plummer, A. A., & Riska, B. (1985). Genetics of mandible form in the mouse. Genetics, 111(3), 555-577.
10. Auffray, J.-C., Alibert, P., Renaud, S., Orth, A., & Bonhomme, F. (1996). Fluctuating asymmetry in Mus musculus subspecific hybridization: Traditional and Procrustes comparative approaches. In Marcus, L. F., Corti, M., Loy, A., Naylor, G. J. P., & Slice, D. E. (Eds.), Advances in Morphometrics: Nato ASI series, series A: life science (pp. 275-284).
11. Badyaev, A. V., & Foresman, K. R. (2004). Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. American Naturalist, 163(6), 868-879. doi:10.1086/386551.
12. Badyaev, A. V., Foresman, K. R., & Fernandes, M. V. (2000). Stress and developmental stability: Vegetation removal causes increased fluctuating asymmetry in shrews. Ecology, 81(2), 336-345.
13. Badyaev, A. V., Foresman, K. R., & Young, R. L. (2005). Evolution of morphological integration: Developmental accommodation of stress-induced variation. American Naturalist, 166(3), 382-395. doi:10.1086/432559.
14. 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. doi:10.1111/j.1469-7580.2006.00644.x.
15. Bookstein, F. L., Streissguth, A. P., Sampson, P. D., Connor, P. D., & Barr, H. M. (2002). Corpus callosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. NeuroImage, 15(1), 233-251. doi:10.1006/nimg.2001.0977.
16. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36(3), 499-516. doi:10.2307/2408096.
17. Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145(1), 63-89. doi:10.1086/285728.
18. Cheverud, J. M. (1996a). Developmental integration and the evolution of pleiotropy. American Zoologist, 36(1), 44-50.
19. 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(1), 5-42. doi:10.1046/j.1420-9101.1996.9010005.x.
20. Cheverud, J. M. (2004). Modular pleiotropic effects of quantitative trait loci on morphological traits. In G. Schlosser & G. P. Wagner (Eds.), Modularity in development and evolution (pp. 132-153). Chicago: University of Chicago Press.
21. Cheverud, J. M., Hartman, S. E., Richtsmeier, J. T., & 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(3), 122-137.
22. Dietz, E. J. (1983). Permutation tests for association between 2 distance matrices. Systematic Zoology, 32(1), 21-26. doi:10.2307/2413216.
23. Dow, M. M., & Cheverud, J. M. (1985). Comparison of distance matrices in studies of population-structure and genetic microdifferentiation-Quadratic assignment. American Journal of Physical Anthropology, 68(3), 367-373. doi:10.1002/ajpa.1330680307.
24. Dow, M. M., & Cheverud, J. M. (1985). Comparison of distance matrices in studies of population-structure and genetic microdifferentiation-Quadratic assignment. American Journal of Physical Anthropology, 68(3), 367-373. doi:10.1002/ajpa.1330680307.
25. Edwards, D. (2000). Introduction to graphical modeling. New York: Springer-Verlag.
26. Edwards, D. (2008). MIM: A program for graphical modeling, version 3.2.0.6. HyperGraph software.
27. Farris, J. S. (1969). On cophenetic correlation coefficient. Systematic Zoology, 18(3), 279. doi:10.2307/2412324.
28. Goswami, A. (2006a). Cranial modularity shifts during mammalian evolution. American Naturalist, 168(2), 270-280. doi:10.1086/505758.
29. Goswami, A. (2006b). Morphological integration in the carnivoran skull. Evolution, 60(1), 169-183.
30. Gould, S. J., & Garwood, R. A. (1969). Levels of integration in mammalian dentitions: An analysis of correlations in Nesophantes micrus (Insectivora) and Oryzomys couesi (Rodentia). Evolution, 23(2), 276. doi:10.2307/2406792.
31. Hall, B. K. (2003). Unlocking the black box between genotype and phenotype: Cell condensations as morphogenetic (modular) units. Biology and Philosophy, 18(2), 219-247. doi:10.1023/A:1023984018531.
32. Hall, B. K., & Miyake, T. (2000). All for one and one for all: Condensations and the initiation of skeletal development. BioEssays, 22(2), 138-147. doi:10.1002/(SICI)1521-1878(200002)22:2<138::AID-BIES5>3.0.CO;2-4.
33. Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. L. (2004). Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 302B(3), 207-225. doi:10.1002/jez.b.21002.
34. Herring, S. W., Rafferty, K. L., Liu, Z. J., & Marshall, C. D. (2001). Jaw muscles and the skull in mammals: The biomechanics of mastication. Comparative Biochemistry and Physiology. A. Comparative Physiology, 131, 207-219.
35. Hood, G. M. (2008). PopTools version 3.0.3. Available at: http://www.cse.csiro.au/poptools/.
36. Jojic, V., Blagojevic, J., Ivanovic, A., Bugarski-Stanojevic, V., & Vujosevic, M. (2007). Morphological integration of the mandible in yellow-necked field mice: The effects of B chromosomes. Journal of Mammalogy, 88(3), 689-695. doi:10.1644/06-MAMM-A-019R1.1.
37. Kaufman, L., & Rousseeuw, P. (1990). Finding groups in data, an introduction to cluster analysis. New York: Wiley.
38. Klingenberg, C. P. (2004). Integration, modules, and development-Molecules to morphology to evolution. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 213-230). New York: Oxford University Press.
39. Klingenberg, C. P. (2005). Developmental constraints, modules, and evolvability. In B. Hallgrímsson & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 219-247). San Diego: Elsevier Academic Press.
40. Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., & Beckwith, N. J. (2001). Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings. American Naturalist, 157(1), 11-23. doi:10.1086/317002.
41. Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56(10), 1909-1920.
42. Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution, 52(5), 1363-1375. doi:10.2307/2411306.
43. 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. doi:10.1046/j.1525-142X.2003.03057.x.
44. Klingenberg, C. P., & Zaklan, S. D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54(4), 1273-1285.
45. Lawler, R. R. (2008). Morphological integration and natural selection in the postcranium of wild Verreaux's sifaka (Propithecus verreauxi verreauxi). American Journal of Physical Anthropology, 136(2), 204-213. doi:10.1002/ajpa.20795.
46. Leamy, L. (1984). Morphometric studies in inbred and hybrid house mice. 5. Directional and fluctuating asymmetry. American Naturalist, 123(5), 579-593. doi:10.1086/284225.
47. 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. doi:10.1111/j.1469-7580.2008.00900.x.
48. Magwene, P. M. (2001). New tools for studying integration and modularity. Evolution, 55(9), 1734-1745.
49. Makarenkov, U. (2000). T-Rex, ver. 4.0a1. Available at: http://www.labunix.uqam.ca/~makarenv/trex.html.
50. Makarenkov, V., & Legendre, P. (2004). From a phylogenetic tree to a reticulated network. Journal of Computational Biology, 11(1), 195-212. doi:10.1089/106652704773416966.
51. Makarenkov, V., Legendre, P., & Desdevises, Y. (2004). Modelling phylogenetic relationships using reticulated networks. Zoologica Scripta, 33(1), 89-96. doi:10.1111/j.1463-6409.2004.00141.x.
52. Marquez, E. (2007a). Coriandis. Available at: http://www-personal.umich.edu/~emarquez/morph/index.html.
53. Marquez, E. (2007b). Sage, ver. 1.03. Available at: http://www-personal.umich.edu/~emarquez/morph/index.html.
54. Marquez, E. J. (in press). A statistical framework for testing modularity in multidimensional data. Evolution.
55. 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.
56. Mezey, J. G., Cheverud, J. M., & Wagner, G. P. (2000). Is the genotype-phenotype map modular? A statistical approach using mouse quantitative trait loci data. Genetics, 156(1), 305-311.
57. Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56, 818-836. doi:10.1080/10635150701648029.
58. Mitteroecker, P., & Bookstein, F. (2008). The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62(4), 943-958. doi:10.1111/j.1558-5646.2008.00321.x.
59. 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. doi:10.1111/j.1525-142X.2005.05047.x.
60. Moss, M. L. (1968). Functional cranial analysis of mammalian mandibular ramal morphology. Acta Anatomica, 71(3), 423. doi:10.1159/000143198.
61. Moss, M. L., & Salentijn, L. (1969). Primary role of functional matrices in facial growth. American Journal of Orthodontics, 55(6), 566-577. doi:10.1016/0002-9416(69)90034-7.
62. Neale, M. C., Boker, S. M., Xie, G., & Maes, H. H. (2003). Mx: Statistical modeling. Richmond, VA: Department of Psychiatry, Virginia Commonwealth University.
63. Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17, 391-421. doi:10.1146/annurev.es.17.110186.002135.
64. Polanski, J. M., & Franciscus, R. G. (2006). Patterns of craniofacial integration in extant Homo, Pan, and Gorilla. American Journal of Physical Anthropology, 131(1), 38-49. doi:10.1002/ajpa.20421.
65. Ross, C. F., & Ravosa, M. J. (1993). Basicranial flexion, relative brain size and facial kyphosis in nonhuman primates. American Journal of Physical Anthropology, 91(3), 305-324. doi:10.1002/ajpa.1330910306.
66. Sampson, P. D., Bookstein, F. L., Sheehan, H., & Bolson, E. L. (1996). Eigenshape analysis of left ventricular outlines from contrast ventriculograms. In L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor, & D. E. Slice (Eds.), Advances in morphometrics, series A: Life science (pp. 131-152). New York: Nato ASI Series.
67. Sattath, S., & Tversky, A. (1977). Additive similarity trees. Psychometrika, 42(3), 319-345. doi:10.1007/BF02293654.
68. Sheets, D. H. (2003). Semiland6. Available at: http://www.canisius.edu/~sheets/morphsoft.html.
69. Sheets, H. D., Kim, K., & Mitchell, C. E. (2004). A combined landmark and outline-based approach to ontogenetic shape change in the Ordovician trilobite Triarthrus becki. In A. M. T. Elewa (Ed.), Morphometrics: Applications in biology and paleontology (pp. 67-82). New York: Springer.
70. Sneath, P. H. A., & Sokal, R. R. (1973). Numerical taxonomy. San Francisco: W. H. Freeman.
71. Strait, D. S., Richmond, B. G., Spencer, M. A., Ross, C. F., Dechow, P. C., & Wood, B. A. (2007). Masticatory biomechanics and its relevance to early hominid phylogeny: An examination of palatal thickness using finite-element analysis. Journal of Human Evolution, 52(5), 585-599. doi:10.1016/j.jhevol.2006.11.019.
72. Thorington, R. W., & Darrow, K. (1996). Jaw muscles of old world squirrels. Journal of Morphology, 230(2), 145-165. doi:10.1002/(SICI)1097-4687(199611)230:2<145::AID-JMOR3>3.0.CO;2-G.
73. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36(1), 36-43.
74. Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967-976. doi:10.2307/2410639.
75. Ward, J. H. (1963). Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58, 236-244. doi:10.2307/2282967.
76. Whittaker, J. (1990). Graphical models in applied multivariate statistics. New York: Wiley.
77. Wilkinson, L. (2000). Systat version 10. San Jose: Systat Software Inc.
78. Willmore, K. E., Zelditch, M. L., Young, N., Ah-Seng, A., Lozanoff, S., & Hallgrímsson, B. (2006). Canalization and developmental stability in the brachyrrhine mouse. Journal of Anatomy, 208(3), 361-372. doi:10.1111/j.1469-7580.2006.00527.x.
79. Young, N. (2004). Modularity and integration in the hominoid scapula. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 302B(3), 226-240. doi:10.1002/jez.b.21003.
80. Young, N. M., & Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59(12), 2691-2704.
81. Zelditch, M. L. (1987). Evaluating models of developmental integration in the laboratory rat using confirmatory factor analysis. Systematic Zoology, 36(4), 368-380. doi:10.2307/2413401.
82. Zelditch, M. L., & Carmichael, A. C. (1989). Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fulviventer. Evolution, 43(4), 814-824. doi:10.2307/2409309.
83. Zelditch, M. L., Wood, A. R., Bonett, R. M., & Swiderski, D. L. (2008). Modularity of the rodent mandible: Integrating bones, muscles and teeth. Evolution & Development (in press).