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Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape

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Abstract

The mammalian mandible is a developmentally modular but functionally integrated system. Whether morphological integration can evolve to match the optimal pattern of functional integration may depend on the developmental origin of integration, specifically, on the role that direct epigenetic interactions play in shaping integration. These interactions are hypothesized to integrate modules and also to be highly conservative, potentially constraining the evolution of integration. Using the fox squirrel (Sciurus niger) mandible as a model system, we test five a priori developmental hypotheses that predict mandibular integration and we also explore for correlations between shapes of mandibular regions not anticipated by any of the developmental models. To determine whether direct epigenetic interactions are highly conserved in rodents, we examine the correlation structure of fluctuating asymmetry, and compare integration patterns between fox squirrels and prairie deer mice (Peromyscus maniculatus bairdii). In fox squirrels, we find a correlation structure unanticipated by all a priori developmental models: adjacent parts along the proximodistal jaw axis are correlated whereas more distant ones are not. The most notable exception is that the shape of the anterior incisor alveolus is correlated with the shape of the ramus (FA component) or coronoid (symmetric component). Those exceptions differ between species; in prairie deer mice, the molar alveolus is connected to more parts, and the incisor alveolus to fewer, than in fox squirrels. The structure of integration suggests that the mandible cannot be decomposed into parts but rather is a single connected unit, a result consistent with its functional integration. That match between functional and developmental integration may arise, at least in part, from function-induced growth, building developmental integration into the functional system and enabling direct epigenetic interactions to evolve when function does.

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References

  • Ackermann, R. R., & Cheverud, J. M. (2000). Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlation and common principal component analysis. American Journal of Physical Anthropology, 111(4), 489–501. doi:10.1002/(SICI)1096-8644(200004)111:4<489::AID-AJPA5>3.0.CO;2-U.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Atchley, W. R., Plummer, A. A., & Riska, B. (1985). Genetics of mandible form in the mouse. Genetics, 111(3), 555–577.

    PubMed  CAS  Google Scholar 

  • 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).

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Bastir, M., Rosas, A., & O’Higgins, P. (2006). Craniofacial levels and the morphological maturation of the human skull. Journal of Anatomy, 209(5), 637–654. doi:10.1111/j.1469-7580.2006.00644.x.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36(3), 499–516. doi:10.2307/2408096.

    Google Scholar 

  • Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145(1), 63–89. doi:10.1086/285728.

    Article  Google Scholar 

  • Cheverud, J. M. (1996a). Developmental integration and the evolution of pleiotropy. American Zoologist, 36(1), 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(1), 5–42. doi:10.1046/j.1420-9101.1996.9010005.x.

    Article  Google Scholar 

  • 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.

  • 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.

    PubMed  CAS  Google Scholar 

  • Dietz, E. J. (1983). Permutation tests for association between 2 distance matrices. Systematic Zoology, 32(1), 21–26. doi:10.2307/2413216.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Edwards, D. (2000). Introduction to graphical modeling. New York: Springer-Verlag.

    Google Scholar 

  • Edwards, D. (2008). MIM: A program for graphical modeling, version 3.2.0.6. HyperGraph software.

  • Farris, J. S. (1969). On cophenetic correlation coefficient. Systematic Zoology, 18(3), 279. doi:10.2307/2412324.

    Article  Google Scholar 

  • Goswami, A. (2006a). Cranial modularity shifts during mammalian evolution. American Naturalist, 168(2), 270–280. doi:10.1086/505758.

    Article  PubMed  Google Scholar 

  • Goswami, A. (2006b). Morphological integration in the carnivoran skull. Evolution, 60(1), 169–183.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Hood, G. M. (2008). PopTools version 3.0.3. Available at: http://www.cse.csiro.au/poptools/.

  • 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.

    Article  Google Scholar 

  • Kaufman, L., & Rousseeuw, P. (1990). Finding groups in data, an introduction to cluster analysis. New York: Wiley.

    Google Scholar 

  • 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.

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56(10), 1909–1920.

    PubMed  Google Scholar 

  • 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.

    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. doi:10.1046/j.1525-142X.2003.03057.x.

    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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lieberman, D. E., Hallgrímsson, B., Liu, W., Parsons, T. E., & Jamniczky, H. A. (2008). Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: Testing a new model using mice. Journal of Anatomy, 212(6), 720–735. doi:10.1111/j.1469-7580.2008.00900.x.

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Makarenkov, U. (2000). T-Rex, ver. 4.0a1. Available at: http://www.labunix.uqam.ca/~makarenv/trex.html.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Marquez, E. (2007a). Coriandis. Available at: http://www-personal.umich.edu/~emarquez/morph/index.html.

  • Marquez, E. (2007b). Sage, ver. 1.03. Available at: http://www-personal.umich.edu/~emarquez/morph/index.html.

  • Marquez, E. J. (in press). A statistical framework for testing modularity in multidimensional data. Evolution.

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56, 818–836. doi:10.1080/10635150701648029.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Monteiro, L. R., Bonato, V., & dos Reis, S. F. (2005). Evolutionary integration and morphological diversification in complex morphological structures: Mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evolution & Development, 7(5), 429–439. doi:10.1111/j.1525-142X.2005.05047.x.

    Article  Google Scholar 

  • Moss, M. L. (1968). Functional cranial analysis of mammalian mandibular ramal morphology. Acta Anatomica, 71(3), 423. doi:10.1159/000143198.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Neale, M. C., Boker, S. M., Xie, G., & Maes, H. H. (2003). Mx: Statistical modeling. Richmond, VA: Department of Psychiatry, Virginia Commonwealth University.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Sattath, S., & Tversky, A. (1977). Additive similarity trees. Psychometrika, 42(3), 319–345. doi:10.1007/BF02293654.

    Article  Google Scholar 

  • Sheets, D. H. (2003). Semiland6. Available at: http://www.canisius.edu/~sheets/morphsoft.html.

  • 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.

    Google Scholar 

  • Sneath, P. H. A., & Sokal, R. R. (1973). Numerical taxonomy. San Francisco: W. H. Freeman.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36(1), 36–43.

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967–976. doi:10.2307/2410639.

    Google Scholar 

  • Ward, J. H. (1963). Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58, 236–244. doi:10.2307/2282967.

    Article  Google Scholar 

  • Whittaker, J. (1990). Graphical models in applied multivariate statistics. New York: Wiley.

    Google Scholar 

  • Wilkinson, L. (2000). Systat version 10. San Jose: Systat Software Inc.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

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Acknowledgements

We are grateful to P. Myers of the University of Michgan Museum of Zoology Mammal Division for access to the specimens used in this study and to A. Dengate for his assistance with photography.

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  1. Museum of Paleontology, University of Michigan, Ann Arbor, MI, 48109, USA

    Miriam Leah Zelditch & Aaron R. Wood

  2. Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI, 48109, USA

    Donald L. Swiderski

  3. Museum of Zoology, University of Michigan, Ann Arbor, MI, 48109, USA

    Donald L. Swiderski

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  1. Miriam Leah Zelditch
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Zelditch, M.L., Wood, A.R. & Swiderski, D.L. Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape. Evol Biol 36, 71–87 (2009). https://doi.org/10.1007/s11692-008-9034-7

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