Craniofacial variability and modularity in macaques and mice
Abstract
Evolutionary developmental biology of primates will be driven largely by the developmental biology of the house mouse. Inferences from how known developmental perturbations produce phenotypic effects in model organisms, such as mice, to how the same perturbations would affect craniofacial form in primates must be informed by comparisons of phenotypic variation and variability in mice and the primate species of interest. We use morphometric methods to compare patterns of cranial variability in homologous datasets obtained for two strains of laboratory mice and rhesus macaques. C57BL/6J represents a common genetic background for transgenic models. A/WySnJ mice exhibit altered facial morphology which results from reduction in the growth of the maxillary process during formation of the face. This is relevant to evolutionary changes in facial prognathism in nonhuman primate and human evolution. Rhesus macaques represent a nonhuman primate about which a great deal of phenotypic and genetic information is available. We find significant similarities in covariation patterns between the C57BL/6J mice and macaques. Among-trait variation in genetic and phenotypic variances are fairly concordant among the three groups, but among-trait variation in developmental stability is not. Finally, analysis of modularity based on phenotypic and genetic correlations did not reveal a consistent pattern in the three groups. We discuss the implications of these results for the study of evolutionary developmental biology of primates and outline a research strategy for integrating mouse genomics and developmental biology into this emerging field.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Morphological integration is not absolute but organized in units that are relatively independent while participating to generate a structure that acts as a functional whole.
“Nonetheless, this integration is not absolute but organized in units that are relatively independent while participating to generate a structure that act as functional whole.”
From Morphological consequences of artificial cranial deformation: Modularity and integration (2020) · cites this paper as [14]
Cites
Applied Multivariate Statistical Analysis.
Johnson, A., & Wichern, D. W. (1988) · Biometrics · doi:10.2307/2531616 · Cited by 11,374 · see citing works
QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY
Lande, R. (1979) · Evolution · doi:10.1111/j.1558-5646.1979.tb04694.x · Cited by 2,648 · see citing works
Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry
Lande, R. (1979) · Evolution · doi:10.2307/2407630 · Cited by 2,648 · see citing works
FLUCTUATING ASYMMETRY: Measurement, Analysis, Patterns
Palmer, A. R., & Strobeck, C. (1986) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.17.110186.002135 · Cited by 2,131 · see citing works
Applied Multivariate Statistical Analysis
Ziegel, E. R., Johnson, R. A., & Wichern, D. W. (1999) · Technometrics · doi:10.2307/1271011 · Cited by 1,564 · see citing works
Evolutionary quantitative genetics
(1998) · Choice Reviews Online · doi:10.5860/choice.35-5054 · Cited by 1,307 · see citing works
Fluctuating asymmetry analyses: a primer
Palmer, A. R. (1994) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-0830-0_26 · Cited by 998 · see citing works
Klingenberg, C. P., & McIntyre, G. S. (1998) · Evolution · doi:10.1111/j.1558-5646.1998.tb02018.x · Cited by 945 · see citing works
PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM
Cheverud, J. M. (1982) · Evolution · doi:10.1111/j.1558-5646.1982.tb05070.x · Cited by 859 · see citing works
A COMPARISON OF GENETIC AND PHENOTYPIC CORRELATIONS
Cheverud, J. M. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb02514.x · Cited by 839 · see citing works
Homologues, Natural Kinds and the Evolution of Modularity
Wagner, G. P. (1996) · American Zoologist · doi:10.1093/icb/36.1.36 · Cited by 837 · see citing works
The primary role of functional matrices in facial growth
Moss, M. L., & Salentijn, L. (1969) · American Journal of Orthodontics · doi:10.1016/0002-9416(69)90034-7 · Cited by 820 · see citing works
Tissue origins and interactions in the mammalian skull vault.
Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M., & Morriss-Kay, G. M. (2002) · Developmental Biology · doi:10.1006/dbio.2001.0487 · Cited by 782 · see citing works
Developmental Integration and the Evolution of Pleiotropy
Cheverud, J. M. (1996) · American Zoologist · doi:10.1093/icb/36.1.44 · Cited by 759 · see citing works
Evolutionary Developmental Biology
(2021) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(21)x0002-6 · Cited by 678 · see citing works
Etterson, J. R. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01726.x · Cited by 639 · see citing works
Evolutionary Developmental Biology
Hall, B. K. (1999) · Springer eBooks · doi:10.1007/978-94-011-3961-8 · Cited by 538 · see citing works
The primate cranial base: Ontogeny, function, and integration
Lieberman, D. E., Ross, C. F., & Ravosa, M. J. (2000) · American Journal of Physical Anthropology · doi:10.1002/1096-8644(2000)43:31+ · Cited by 535 · see citing works
Fluctuating Asymmetry Analyses Revisited
Palme, R., & Strobeck, C. (2003) · doi:10.1093/oso/9780195143454.003.0017 · Cited by 487 · see citing works
PERSPECTIVE: EVOLUTIONARY DEVELOPMENTAL BIOLOGY AND THE PROBLEM OF VARIATION
Stern, D. L. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00544.x · Cited by 483 · see citing works
Marroig, G., & Cheverud, J. M. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00770.x · Cited by 425 · see citing works
The Evolution of Developmental Pathways
Gagneux, P. (2002) · Journal of Heredity · doi:10.1093/jhered/93.6.460 · Cited by 414 · see citing works
The Evolution of Developmental Pathways
Wilkins, A. S. (2001) · Cited by 398 · see citing works
Canalization, developmental stability, and morphological integration in primate limbs
Hallgrímsson, B., Willmore, K. E., & Hall, B. K. (2002) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10182 · Cited by 391 · see citing works
Self-citationGenes, Development and Evolution of the Placenta
Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H., & Kingdom, J. C. (2003) · Placenta · doi:10.1053/plac.2002.0887 · Cited by 348 · see citing works
Morphological Integration in the Saddle-Back Tamarin (Saguinus fuscicollis) Cranium
Cheverud, J. M. (1995) · The American Naturalist · doi:10.1086/285728 · Cited by 336 · see citing works
Basicranial influence on overall cranial shape
Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000) · Journal of Human Evolution · doi:10.1006/jhev.1999.0335 · Cited by 335 · see citing works
Klingenberg, C. P., Mebus, K., & Auffray, J. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03057.x · Cited by 333 · see citing works
An Invariant Approach to Statistical Analysis of Shapes
Lele, S. R., & Richtsmeier, J. T. (2001) · Chapman & Hall/CRC eBooks · doi:10.1201/9781420036176 · Cited by 308 · see citing works
Keywords and concepts in evolutionary developmental biology
(2003) · Choice Reviews Online · doi:10.5860/choice.41-1538 · Cited by 274 · see citing works
Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., & Beckwith, N. J. (2001) · The American Naturalist · doi:10.1086/317002 · Cited by 257 · see citing works
Klingenberg, C. P., Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2001) · Genetics · doi:10.1093/genetics/157.2.785 · Cited by 239 · see citing works
MORPHOLOGICAL INTEGRATION BETWEEN DEVELOPMENTAL COMPARTMENTS IN THE DROSOPHILA WING
Klingenberg, C. P., & Zaklan, S. D. (2000) · Evolution · doi:10.1554/0014-3820(2000)054[1273:mibdci]2.0.co;2 · Cited by 237 · see citing works
Lieberman, D. E., & McCarthy, R. C. (1999) · Journal of Human Evolution · doi:10.1006/jhev.1998.0287 · Cited by 221 · see citing works
Paigen, K., & Eppig, J. T. (2000) · Mammalian Genome · doi:10.1007/s003350010152 · Cited by 219 · see citing works
How should we explain variation in the genetic variance of traits?
Houle, D. (1998) · Genetica · doi:10.1023/a:1017034925212 · Cited by 219 · see citing works
NEW TOOLS FOR STUDYING INTEGRATION AND MODULARITY
Magwene, P. M. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00823.x · Cited by 213 · see citing works
MORPHOLOGICAL INTEGRATION BETWEEN DEVELOPMENTAL COMPARTMENTS IN THE DROSOPHILA WING
Klingenberg, C. P., & Zaklan, S. D. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00560.x · Cited by 210 · see citing works
How should we explain variation in the genetic variance of traits?
Houle, D. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_20 · Cited by 204 · see citing works
Moss, M. L. (1962) · Medical Entomology and Zoology · Cited by 199 · see citing works
On Comparing Coefficients of Variation
Lande, R. (1977) · Systematic Zoology · doi:10.2307/2412845 · Cited by 193 · see citing works
Euclidean Distance Matrix Analysis (EDMA): Estimation of mean form and mean form difference
Lele, S. R. (1993) · Mathematical Geology · doi:10.1007/bf00890247 · Cited by 192 · see citing works
Keywords and Concepts in Evolutionary Developmental Biology
(2006) · Harvard University Press eBooks · doi:10.2307/j.ctv228vqrq · Cited by 173 · see citing works
On Comparing Coefficients of Variation
Lande, R. (1977) · Systematic Biology · doi:10.1093/sysbio/26.2.214 · Cited by 167 · see citing works
Multiple functions of Dlx genes
Merlo, G. R., Zerega, B., Paleari, L., Trombino, S., Mantero, S., & Levi, G. (2000) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11061425 · Cited by 162 · see citing works
Independence between developmental stability and canalization in the skull of the house mouse
Debat, V., Alibert, P., David, P., Paradis, E., & Auffray, J. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1017 · Cited by 162 · see citing works
Homology and Embryonic Development
Hall, B. K. (1995) · Springer eBooks · doi:10.1007/978-1-4615-1847-1_1 · Cited by 127 · see citing works
The genetic basis of modularity in the development and evolution of the vertebrate dentition
Stock, D. W. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0917 · Cited by 115 · see citing works
Revised nomenclature for strain 129 mice
Festing, M. F. W., Simpson, E. M., Davisson, M. T., & Mobraaten, L. E. (1999) · Mammalian Genome · doi:10.1007/s003359901099 · Cited by 98 · see citing works
Amplified developmental instability in Down's syndrome
Shapiro, B. L. (1975) · Annals of Human Genetics · doi:10.1111/j.1469-1809.1975.tb00632.x · Cited by 83 · see citing works
Cheverud, J. M., Hartman, S. E., Richtsmeier, J. T., & Atchley, W. R. (1991) · PubMed · Cited by 73 · see citing works
Genomic structure and functional control of the Dlx3 - 7 bigene cluster
Sumiyama, K., Irvine, S. Q., Stock, D. W., Weiss, K. M., Kawasaki, K., Shimizu, N., Shashikant, C. S., Miller, W., & Ruddle, F. H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012584999 · Cited by 71 · see citing works
PHYLOGENETIC ANALYSIS OF PHENOTYPIC COVARIANCE STRUCTURE. II. RECONSTRUCTING MATRIX EVOLUTION
Steppan, S. J. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb02445.x · Cited by 71 · see citing works
Craniofacial development in the absence of muscle contraction.
Herring, S., & Lakars, T. C. (1982) · PubMed · Cited by 71 · see citing works
DEVELOPMENTAL INTERACTIONS AND THE CONSTITUENTS OF QUANTITATIVE VARIATION
Wolf, J. B., Frankino, W. A., Agrawal, A. F., Brodie, E. D., & Moore, A. J. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb01289.x · Cited by 69 · see citing works
Understanding craniofacial anomalies : the etiopathogenesis of craniosynostoses and facial clefting
Mooney, M. P., & Siegel, M. I. (2002) · Cited by 58 · see citing works
Haag, E. S., & True, J. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00627.x · Cited by 57 · see citing works
Wang, K. Y., Juriloff, D. M., & Diewert, V. M. (1996) · PubMed · Cited by 57 · see citing works
Unravelling the complex genetics of cleft lip in the mouse model
Juriloff, D. M., Harris, M. J., & Brown, C. J. (2001) · Mammalian Genome · doi:10.1007/s003350010284 · Cited by 56 · see citing works
Klingenberg, Badyaev, Sowry, & Beckwith (2001) · The American Naturalist · doi:10.2307/3079085 · Cited by 56 · see citing works
Regulation of Dlx3 gene expression in visceral arches by evolutionarily conserved enhancer elements
Sumiyama, K., & Ruddle, F. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0530119100 · Cited by 46 · see citing works
Bacon, A. (2000) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(200004)111:4 · Cited by 39 · see citing works
A morphometric analysis of craniofacial growth in cleft lip and noncleft mice.
Ky, W., & Diewert, V. M. (1992) · PubMed · Cited by 38 · see citing works
Diewert, V. M. (1982) · PubMed · Cited by 36 · see citing works
Invariance, Identifiability, and Morphometrics
Lele, S. R., & McCulloch, C. E. (2002) · Journal of the American Statistical Association · doi:10.1198/016214502388618609 · Cited by 31 · see citing works
Midfacial Retrusion in Adult Brachyrrhine Mice
Lozanoff, S. (1993) · Cells Tissues Organs · doi:10.1159/000147492 · Cited by 26 · see citing works
Frontonasal dysplasia in 3H1 Br/Br mice
McBratney‐Owen, B., Margaryan, E., Ma, W., Urbán, Z., & Lozanoff, S. (2003) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.10034 · Cited by 26 · see citing works
Fluctuating Asymmetry, Developmental Instability, and Fitness: Toward Model-Based Interpretation
Gangestad, S. W., & Thornhill, R. (2003) · doi:10.1093/oso/9780195143454.003.0005 · Cited by 24 · see citing works
Animal Models of Facial Clefting: Experimental, Congenital, and Transgenic
Diewert, V. M., & Lozanoff, S. (2002) · doi:10.1002/0471221953.ch10 · Cited by 21 · see citing works
DEVELOPMENTAL INTERACTIONS AND THE CONSTITUENTS OF QUANTITATIVE VARIATION
Wolf, J. B., Frankino, W. A., Agrawal, A. F., et al. (2001) · Evolution · doi:10.1554/0014-3820(2001)055[0232:diatco]2.0.co;2 · Cited by 16 · see citing works
Experimental approaches to the determination of genetic variability
Festing, M. F. W. (2001) · Toxicology Letters · doi:10.1016/s0378-4274(01)00281-8 · Cited by 15 · see citing works
Haag, E. S., & True, J. (2001) · Evolution · doi:10.1554/0014-3820(2001)055[1077:pfmtma]2.0.co;2 · Cited by 15 · see citing works
Stein, G. S., van Wijnen, A. J., Stein, J. L., Lian, J. B., McNeil, S. M., & Pockwinse, S. M. (1999) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(1999)75:32+ · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Morphological integration and developmental modularity
Klingenberg, C. P. (2008) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110054 · Cited by 863 · see citing works
Hallgrímsson, B., Jamniczky, H. A., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., & Marcucio, R. (2009) · Evolutionary Biology · doi:10.1007/s11692-009-9076-5 · Cited by 453 · see citing works
Self-citationStress-induced variation in evolution: from behavioural plasticity to genetic assimilation
Badyaev, A. V. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.3045 · Cited by 442 · see citing works
Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications
Klingenberg, C. P. (2015) · Symmetry · doi:10.3390/sym7020843 · Cited by 441 · see citing works
The macroevolutionary consequences of phenotypic integration: from development to deep time
Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0254 · Cited by 359 · see citing works
Albertson, R. C., Streelman, J. T., Kocher, T. D., & Yelick, P. C. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506649102 · Cited by 325 · see citing works
The Conceptual and Statistical Relationship between Modularity and Morphological Integration
Mitterœcker, P., & Bookstein, F. L. (2007) · Systematic Biology · doi:10.1080/10635150701648029 · Cited by 273 · see citing works
The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)
Goswami, A., & Polly, P. D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009517 · Cited by 271 · see citing works
The evolutionary role of modularity and integration in the Hominoid cranium
Mitteroecker, P., & Bookstein, F. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00321.x · Cited by 267 · see citing works
Kawauchi, S., Calof, A. L., Santos, R., Lopez‐Burks, M. E., Young, C. M., Hoang, M. P., Chua, A., Lao, T., Lechner, M. S., Daniel, J. A., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000650 · Cited by 239 · see citing works
Self-citationEpigenetic interactions and the structure of phenotypic variation in the cranium
Hallgrímsson, B., Lieberman, D. E., Liu, W., Ford‐Hutchinson, A. F., & Jirik, F. R. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00139.x · Cited by 200 · see citing works
Self-citationDoes the skull carry a phylogenetic signal? Evolution and modularity in the guenons
Cardini, A., & Elton, S. (2008) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2008.01011.x · Cited by 201 · see citing works
Cranial integration and modularity: insights into evolution and development from morphometric data
(2013) · Bollettino del CILEA (CILEA) · doi:10.4404/hystrix-24.1-6367 · Cited by 199 · see citing works
Heritability of human cranial dimensions: comparing the evolvability of different cranial regions
Martínez‐Abadías, N., Esparza, M., Sjøvold, T., González‐José, R., Mauro Santos, A., & Hernández, M. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.01015.x · Cited by 192 · see citing works
Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance
Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04025.x · Cited by 188 · see citing works
Phenotypic integration of neurocranium and brain
Richtsmeier, J. T., Aldridge, K. J., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., Yan, P., & Cole, T. M. (2006) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21092 · Cited by 171 · see citing works
Methods for Studying Morphological Integration and Modularity
Goswami, A., & Polly, P. D. (2010) · The Paleontological Society Papers · doi:10.1017/s1089332600001881 · Cited by 163 · see citing works
Lieberman, D. E., Hallgrímsson, B., Liu, W., Parsons, T. E., & Jamniczky, H. A. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00900.x · Cited by 162 · see citing works
Self-citationvon Cramon‐Taubadel, N. (2014) · PubMed · doi:10.4436/jass.91010 · Cited by 146 · see citing works
The morphology of the mouse masticatory musculature
Baverstock, H., Jeffery, N. S., & Cobb, S. N. (2013) · Journal of Anatomy · doi:10.1111/joa.12059 · Cited by 146 · see citing works
A Single Basis for Developmental Buffering of Drosophila Wing Shape
Breuker, C. J., Patterson, J., & Klingenberg, C. P. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000007 · Cited by 139 · see citing works
Zelditch, M. L., & Goswami, A. (2021) · Evolution & Development · doi:10.1111/ede.12390 · Cited by 121 · see citing works
In search of morphological modules: a systematic review
Esteve‐Altava, B. (2016) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12284 · Cited by 114 · see citing works
Gómez‐Robles, A., & Polly, P. D. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01508.x · Cited by 112 · see citing works
Paschetta, C., de Azevedo, S., Castillo, L. D., Martínez‐Abadías, N., Hernández, M., Lieberman, D. E., & González‐José, R. (2009) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21151 · Cited by 110 · see citing works
THE RELATIONSHIP BETWEEN FLUCTUATING ASYMMETRY AND ENVIRONMENTAL VARIANCE IN RHESUS MACAQUE SKULLS
Willmore, K. E., Klingenberg, C. P., & Hallgrímsson, B. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01763.x · Cited by 108 · see citing works
Self-citationZelditch, M. L., Wood, A. R., & Swiderski, D. L. (2008) · Evolutionary Biology · doi:10.1007/s11692-008-9034-7 · Cited by 108 · see citing works
Goswami, A., & Finarelli, J. A. (2016) · Evolution · doi:10.1111/evo.12956 · Cited by 99 · see citing works
Hallgrímsson, B., Brown, J. J. Y., Ford-Hutchinson, A. F., Sheets, H. D., Zelditch, M. L., & Jirik, F. R. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.05075.x · Cited by 104 · see citing works
Self-citationPérez, S. I., & Monteiro, L. R. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00539.x · Cited by 101 · see citing works
Constraints Evolve: Context Dependency of Gene Effects Allows Evolution of Pleiotropy
Pavličev, M., & Cheverud, J. M. (2015) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-120213-091721 · Cited by 95 · see citing works
QUANTITATIVE GENETICS OF SHAPE IN CRICKET WINGS: DEVELOPMENTAL INTEGRATION IN A FUNCTIONAL STRUCTURE
Klingenberg, C. P., Debat, V., & Roff, D. A. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01030.x · Cited by 95 · see citing works
Mouse models and the evolutionary developmental biology of the skull
Hallgrímsson, B., & Lieberman, D. E. (2008) · Integrative and Comparative Biology · doi:10.1093/icb/icn076 · Cited by 95 · see citing works
Self-citationvon Cramon‐Taubadel, N. (2011) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21550 · Cited by 91 · see citing works
Evolution of Morphological Integration: Developmental Accommodation of Stress-Induced Variation
Badyaev, A. V., Foresman, K. R., & Young, R. L. (2005) · The American Naturalist · doi:10.1086/432559 · Cited by 90 · see citing works
Developmental regulation of skull morphology II: ontogenetic dynamics of covariance
Zelditch, M. L., Mezey, J. G., Sheets, H. D., Lundrigan, B. L., & Garland, T. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.05074.x · Cited by 87 · see citing works
Willmore, K. E., Leamy, L. J., & Hallgrímsson, B. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00127.x · Cited by 85 · see citing works
Self-citationMitterœcker, P. (2009) · Evolutionary Biology · doi:10.1007/s11692-009-9075-6 · Cited by 85 · see citing works
Functional and Genetic Integration in the Skulls of Lake Malawi Cichlids
Cooper, W. J., Wernlé, J. D., Mann, K. A., & Albertson, R. C. (2011) · Evolutionary Biology · doi:10.1007/s11692-011-9124-9 · Cited by 75 · see citing works
Morphological integration between the cranial base and the face in children and adults
Gkantidis, N., & Halazonetis, D. J. (2011) · Journal of Anatomy · doi:10.1111/j.1469-7580.2011.01346.x · Cited by 74 · see citing works
Evidence for the Influence of Diet on Cranial Form and Robusticity
Menegaz, R. A., Sublett, S. V., Figueroa, S. D., Hoffman, T. J., Ravosa, M. J., & Aldridge, K. J. (2010) · The Anatomical Record · doi:10.1002/ar.21134 · Cited by 74 · see citing works
Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals
Goswami, A., Polly, P. D., Mock, O. B., & Sánchez-Villagra, M. R. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02477.x · Cited by 66 · see citing works
Devine, J., Aponte, J. D., Katz, D. C., Liu, W., Vercio, L. L., Forkert, N. D., Marcucio, R., Percival, C. J., & Hallgrímsson, B. (2020) · Evolutionary Biology · doi:10.1007/s11692-020-09508-8 · Cited by 59 · see citing works
Self-citationCraniofacial variability and morphological integration in mice susceptible to cleft lip and palate
Hallgrímsson, B., Dorval, C. J., Zelditch, M. L., & German, R. Z. (2004) · Journal of Anatomy · doi:10.1111/j.0021-8782.2004.00356.x · Cited by 65 · see citing works
Self-citationOptic disc morphology - Rethinking shape
Sanfilippo, P. G., Cardini, A., Hewitt, A. W., Crowston, J. G., & Mackey, D. A. (2009) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2009.05.004 · Cited by 59 · see citing works
A MODULAR FRAMEWORK CHARACTERIZES MICRO- AND MACROEVOLUTION OF OLD WORLD MONKEY DENTITIONS
Grieco, T. M., Rizk, O. T., & Hlusko, L. J. (2012) · Evolution · doi:10.1111/j.1558-5646.2012.01757.x · Cited by 56 · see citing works
Laffont, R., Renvoisé, É., Navarro, N., Alibert, P., & Montuire, S. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2009.00332.x · Cited by 55 · see citing works
Effects of cranial integration on hominid endocranial shape
Zollikofer, C. P. E., Bienvenu, T., & de León, M. S. P. (2016) · Journal of Anatomy · doi:10.1111/joa.12531 · Cited by 47 · see citing works
Canalization and developmental stability in the Brachyrrhine mouse
Willmore, K. E., Zelditch, M. L., Young, N. M., Ah-Seng, A. C., Lozanoff, S., & Hallgrímsson, B. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00527.x · Cited by 47 · see citing works
Self-citationDevelopmental plasticity in covariance structure of the skull: effects of prenatal stress
González, P., Hallgrímsson, B., & Oyhenart, E. E. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01326.x · Cited by 43 · see citing works
Self-citationComparison of Mandibular Phenotypic and Genetic Integration between Baboon and Mouse
Willmore, K. E., Roseman, C. C., Rogers, J., Cheverud, J. M., & Richtsmeier, J. T. (2009) · Evolutionary Biology · doi:10.1007/s11692-009-9056-9 · Cited by 46 · see citing works
Self-citationRae, T. C., Viðarsdóttir, U. S., Jeffery, N. S., & Steegmann, A. T. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3629 · Cited by 41 · see citing works
B chromosomes and cranial variability in yellow-necked field mice (Apodemus flavicollis)
Jojić, V., Blagojević, J., & Vujošević, M. (2011) · Journal of Mammalogy · doi:10.1644/10-mamm-a-158.1 · Cited by 40 · see citing works
Modularity of a Cambrian ptychoparioid trilobite cranidium
Webster, M., & Zelditch, M. L. (2011) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00459.x · Cited by 40 · see citing works
Evolutionary Lability of Integration in Cambrian Ptychoparioid Trilobites
Webster, M., & Zelditch, M. L. (2011) · Evolutionary Biology · doi:10.1007/s11692-011-9110-2 · Cited by 40 · see citing works
Creating diversity in mammalian facial morphology: a review of potential developmental mechanisms
Usui, K., & Tokita, M. (2018) · EvoDevo · doi:10.1186/s13227-018-0103-4 · Cited by 40 · see citing works
Craniofacial skeletal response to encephalization: How do we know what we think we know?
Lesciotto, K. M., & Richtsmeier, J. T. (2019) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23766 · Cited by 39 · see citing works
Effects of aneuploidy on skull growth in a mouse model of Down syndrome
Hill, C. A., Reeves, R. H., & Richtsmeier, J. T. (2007) · Journal of Anatomy · doi:10.1111/j.1469-7580.2007.00705.x · Cited by 39 · see citing works
Ivanović, A., & Kalezić, M. L. (2010) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21358 · Cited by 37 · see citing works
Gonzalez, P. N., Oyhenart, E. E., & Hallgrímsson, B. (2011) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21430 · Cited by 36 · see citing works
Self-citationGenetic correlations between mandibular molar cusp areas in baboons
Hlusko, L. J., Do, N., & Mahaney, M. C. (2006) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20528 · Cited by 36 · see citing works
Boughner, J. C., & Hallgrímsson, B. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21383 · Cited by 34 · see citing works
Self-citationSingleton, M. (2012) · Evolutionary Biology · doi:10.1007/s11692-011-9153-4 · Cited by 34 · see citing works
Jojić, V., Blagojević, J., & Vujošević, M. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02612.x · Cited by 31 · see citing works
Postnatal brain and skull growth in an Apert syndrome mouse model
Hill, C. A., Martínez‐Abadías, N., Perrine, S. M. M., Austin, J. R., Wang, Y., Jabs, E. W., Richtsmeier, J. T., & Aldridge, K. J. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.35805 · Cited by 29 · see citing works
A Natural Animal Model System of Craniofacial Anomalies: The Blind Mexican Cavefish
Gross, J. B., & Powers, A. K. (2018) · The Anatomical Record · doi:10.1002/ar.23998 · Cited by 26 · see citing works
Fahlke, J. M., & Hampe, O. (2015) · Die Naturwissenschaften · doi:10.1007/s00114-015-1309-0 · Cited by 27 · see citing works
Neaux, D. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23163 · Cited by 27 · see citing works
Santi, N. A. D., Verzi, D. H., Olivares, A. I., Piñero, P., Morgan, C. C., Medina, M. E., Rivero, D. E., & Tonni, E. P. (2020) · Journal of South American Earth Sciences · doi:10.1016/j.jsames.2020.102499 · Cited by 25 · see citing works
Zelditch, M. L., & Swiderski, D. L. (2023) · Evolutionary Biology · doi:10.1007/s11692-023-09600-9 · Cited by 23 · see citing works
Grieco, T. M., & Rizk, O. T. (2010) · Journal of Morphology · doi:10.1002/jmor.10839 · Cited by 23 · see citing works
López‐Aguirre, C., Pérez‐Torres, J., & Wilson, L. A. B. (2015) · PeerJ · doi:10.7717/peerj.1197 · Cited by 23 · see citing works
Developmental origin underlies evolutionary rate variation across the placental skull
Goswami, A., Noirault, E., Coombs, E. J., Clavel, J., Fabre, A., Halliday, T. J. D., Churchill, M., Curtis, A. A., Watanabe, A., Simmons, N. B., et al. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0083 · Cited by 22 · see citing works
Microstructure of trabecular bone in a mouse model for down syndrome
Parsons, T. E., Ryan, T. M., Reeves, R. H., & Richtsmeier, J. T. (2007) · The Anatomical Record · doi:10.1002/ar.20494 · Cited by 22 · see citing works
Morphological consequences of artificial cranial deformation: Modularity and integration
Püschel, T. A., Friess, M., & Manríquez, G. (2020) · PLOS ONE · doi:10.1371/journal.pone.0227362 · Cited by 22 · see citing works
Shifts in subsistence type and its impact on the human skull's morphological integration
Paschetta, C., de Azevedo, S., González, M. F., Quinto‐Sánchez, M., Cintas, C., Varela, H., Gómez‐Valdés, J., Sánchez‐Mejorada, G., & González‐José, R. (2015) · American Journal of Human Biology · doi:10.1002/ajhb.22746 · Cited by 20 · see citing works
Arístide, L., Bastide, P., dos Reis, S. F., dos Santos, T. M. P., Lopes, R. T., & Pérez, S. I. (2018) · Evolution · doi:10.1111/evo.13609 · Cited by 21 · see citing works
Evolution of Morphological Integration: Developmental Accommodation of Stress-Induced Variation
Badyaev, Foresman, & Young (2005) · The American Naturalist · doi:10.2307/3473316 · Cited by 20 · see citing works
Phylogeny and foraging behaviour shape modular morphological variation in bat humeri
López‐Aguirre, C., Hand, S. J., Koyabu, D. B., Tú, V. T., & Wilson, L. A. B. (2020) · Journal of Anatomy · doi:10.1111/joa.13380 · Cited by 19 · see citing works
Morphological integration of the kinetic skull inNatrixsnakes
Andjelković, M., Tomović, L., & Ivanović, A. (2017) · Journal of Zoology · doi:10.1111/jzo.12477 · Cited by 18 · see citing works
Copes, L. E., Schutz, H., Dlugsoz, E. M., Judex, S., & Garland, T. (2018) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23446 · Cited by 18 · see citing works
Biodiversity and evolution in the light of morphometrics: From patterns to processes
Laffont, R., Firmat, C., Alibert, P., David, B., Montuire, S., & Saucède, T. (2010) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2010.10.004 · Cited by 17 · see citing works
Neaux, D., Guy, F., Gilissen, E., Coudyzer, W., Vignaud, P., & Ducrocq, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057026 · Cited by 16 · see citing works
Evolutionary patterns of cat-like carnivorans unveil drivers of the sabertooth morphology
Chatar, N., Michaud, M., Tamagnini, D., & Fischer, V. (2024) · Current Biology · doi:10.1016/j.cub.2024.04.055 · Cited by 15 · see citing works
Physical Anthropology at the Caribbean Primate Research Center: Past, Present, and Future
Dunbar, D. C. (2011) · Springer eBooks · doi:10.1007/978-1-4614-1046-1_1 · Cited by 15 · see citing works
EVOLUTION OF SEXUAL DIMORPHISM IN MUSTELIDS
Berdnikovs, S. (2005) · Cited by 14 · see citing works
Palate Variation and Evolution in New World Leaf-Nosed and Old World Fruit Bats (Order Chiroptera)
Sorensen, D. W., Butkus, C. E., Cooper, L. N., Cretekos, C. J., Rasweiler, J. J., & Sears, K. E. (2014) · Evolutionary Biology · doi:10.1007/s11692-014-9291-6 · Cited by 14 · see citing works
Hlusko, L. J., & Mahaney, M. C. (2006) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2006.09.008 · Cited by 14 · see citing works
Monson, T. A., Brasil, M., Stratford, D., & Hlusko, L. J. (2017) · Palaeontologia Electronica · doi:10.26879/690 · Cited by 13 · see citing works
Patterns and magnitudes of craniofacial covariation in extant cercopithecids
Monson, T. A. (2020) · The Anatomical Record · doi:10.1002/ar.24398 · Cited by 12 · see citing works
Modularity and cranial integration across ontogenetic stages in Martino’s vole, Dinaromys bogdanovi
Klenovšek, T., & Jojić, V. (2016) · Bijdragen tot de Dierkunde · doi:10.1163/18759866-08503002 · Cited by 12 · see citing works
MusMorph, a database of standardized mouse morphology data for morphometric meta-analyses
Devine, J., Vidal‐García, M., Liu, W., Neves, A., Vercio, L. L., Green, R. M., Richbourg, H. A., Marchini, M., Unger, C. M., Nickle, A. C., et al. (2022) · Scientific Data · doi:10.1038/s41597-022-01338-x · Cited by 12 · see citing works
Self-citationBuilding blocks of a fish head: Developmental and variational modularity in a complex system
Lehoux, C., & Cloutier, R. (2015) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22639 · Cited by 11 · see citing works
Băncilă, R. I., Plăiaş̧u, R., Tudor, M., Samoilă, C., & Cogălniceanu, D. (2012) · Chelonian Conservation and Biology · doi:10.2744/ccb-0956.1 · Cited by 11 · see citing works
Abadías, N. M. (2007) · Cited by 11 · see citing works
Ferreira‐Cardoso, S., Claude, J., Goswami, A., Delsuc, F., & Hautier, L. (2022) · BMC Ecology and Evolution · doi:10.1186/s12862-022-02030-9 · Cited by 10 · see citing works
Development Shapes a Consistent Inbreeding Effect in Mouse Crania of Different Line Crosses
Pavličev, M., Mitterœcker, P., González, P., Rolian, C., Jamniczky, H. A., de Villena, F. P., Marcucio, R., Spritz, R. A., & Hallgrímsson, B. (2016) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22722 · Cited by 9 · see citing works
Self-citationPhylogeny, Ecology, and Morphological Evolution in the Atelid Cranium
Bjarnason, A., Soligo, C., & Elton, S. (2015) · International Journal of Primatology · doi:10.1007/s10764-015-9839-z · Cited by 8 · see citing works
Complexity, Modularity, and Integration in the Human Head. The Evolution of the Human Head
Ross, C. F. (2012) · Journal of Human Evolution · doi:10.1016/j.jhevol.2012.08.010 · Cited by 8 · see citing works
Ontogenetic changes in magnitudes of integration in the macaque skull
Jung, H., Simons, E. A., & von Cramon‐Taubadel, N. (2020) · American Journal of Physical Anthropology · doi:10.1002/ajpa.24119 · Cited by 7 · see citing works
- Authors
- Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. L.
- Affiliations
- University of Calgary (CA)
- Corresponding author
- Hallgrímsson, Benedikt
- Venue
- Journal of Experimental Zoology Part B Molecular and Developmental Evolution
- Publisher
- Wiley
- Published
- 2004-05-15
- Volume
- 302B
- Issue
- 3
- Pages
- 207-225
- ISSN
- 1552-5007 (ISSN-L)
- 1552-5015
- OpenAlex
- W2224335487
- Cited by
- 134
- References
- 74
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 10 · 2022: 3 · 2021: 4 · 2020: 7 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 8 · 2015: 11 · 2014: 4 · 2013: 6 · 2012: 7
- FWCI
- 11.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Experimental Zoology Part B Molecular and Developmental Evolution (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NSERC (238992-02)
- CFI (3923)
- Alberta Innovation and Science (URSI-01-103-RI to B.H.)
- Topics
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Craniofacial Disorders and Treatments
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- modularity, skull morphology, rhesus monkeys, house mouse, C57BL/6J mice, maxillary process, developmental stability, covariation, evolutionary developmental biology
- MeSH terms
- Animals, Biometry, Body Weights and Measures, Bone Development, Biological Evolution, Macaca mulatta, Mice, Mutant Strains, Phenotype, Skull, Species Specificity, Principal Component Analysis, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review