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The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)
Open accessAbstract
BACKGROUND: Although variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution. PRINCIPAL FINDINGS: We used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis. CONCLUSIONS: This analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.
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“A similar pattern has been demonstrated in the mammal cranium (14).”
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Cites
Geometric morphometrics for biologists: a primer
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004) · Cited by 3,321
American Journal of Physical Anthropology
American Association of Physical Anthropologists (2006) · American Journal of Physical Anthropology · doi:10.1002/(issn)1096-8644 · Cited by 2,705
PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY
Wagner, G. P., & Altenberg, L. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb02339.x · Cited by 2,118
Annual Review of Ecology and Systematics
Lawton, J. H., & Johnston, R. F. (1974) · Journal of Animal Ecology · doi:10.2307/3390 · Cited by 1,960
Evolution at Two Levels: On Genes and Form
Carroll, S. B. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030245 · Cited by 882
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
Homologues, Natural Kinds and the Evolution of Modularity
Wagner, G. P. (1996) · American Zoologist · doi:10.1093/icb/36.1.36 · Cited by 802
Developmental Integration and the Evolution of Pleiotropy
Cheverud, J. M. (1996) · American Zoologist · doi:10.1093/icb/36.1.44 · Cited by 759
Quantitative genetics and developmental constraints on evolution by selection
Cheverud, J. M. (1984) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(84)80050-8 · Cited by 715
The Evolution of Morphological Diversity
Foote, M. (1997) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.28.1.129 · Cited by 655
A MODEL FOR DEVELOPMENT AND EVOLUTION OF COMPLEX MORPHOLOGICAL STRUCTURES
Atchley, W. R., & Hall, B. K. (1991) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1991.tb01138.x · Cited by 587
Proceedings of the Michigan Morphometrics Workshop.
Warheit, K. I., Rohlf, F. J., & Bookstein, F. L. (1992) · Systematic Biology · doi:10.2307/2992576 · Cited by 564
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
Spratt, N. T., Olson, E. C., & Miller, R. L. (1959) · AIBS Bulletin · doi:10.2307/1292755 · Cited by 509
Marroig, G., & Cheverud, J. M. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00770.x · Cited by 425
Marroig, G., & Cheverud, J. M. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01049.x · Cited by 357
Morphological Integration in the Saddle-Back Tamarin (Saguinus fuscicollis) Cranium
Cheverud, J. M. (1995) · The American Naturalist · doi:10.1086/285728 · Cited by 336
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
Klingenberg, C. P., Mebus, K., & Auffray, J. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03057.x · Cited by 333
Cheverud, J. M., Rutledge, J. J., & Atchley, W. R. (1983) · Evolution · doi:10.1111/j.1558-5646.1983.tb05619.x · Cited by 297
Cranial modularity shifts during mammalian evolution
Goswami, A. (2006) · The American Naturalist · doi:10.1086/505758 · Cited by 280
Self-citationThe Conceptual and Statistical Relationship between Modularity and Morphological Integration
Mitterœcker, P., & Bookstein, F. L. (2007) · Systematic Biology · doi:10.1080/10635150701648029 · Cited by 273
Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., & Beckwith, N. J. (2001) · The American Naturalist · doi:10.1086/317002 · Cited by 257
Klingenberg, C. P., Leamy, L. J., & Cheverud, J. M. (2004) · Genetics · doi:10.1534/genetics.166.4.1909 · Cited by 249
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
QUANTITATIVE GENETICS OF GEOMETRIC SHAPE IN THE MOUSE MANDIBLE
Klingenberg, C. P., & Leamy, L. J. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00747.x · Cited by 228
Cheverud, J. M. (1996) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1996.9010005.x · Cited by 222
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
Hierarchical nature of morphological integration and modularity in the human posterior face
Bastir, M., & Rosas, A. (2005) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20191 · Cited by 194
PLEIOTROPIC EFFECTS OF INDIVIDUAL GENE LOCI ON MANDIBULAR MORPHOLOGY
Cheverud, J. M., Routman, E. J., & Irschick, D. J. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb05122.x · Cited by 189
Morphometrics and the role of the phenotype in studies of the evolution of developmental mechanisms
Klingenberg, C. P. (2002) · Gene · doi:10.1016/s0378-1119(01)00867-8 · Cited by 178
Wesley‐Hunt, G. D., & Flynn, J. J. (2005) · Journal of Systematic Palaeontology · doi:10.1017/s1477201904001518 · Cited by 175
Beyond heterochrony : the evolution of development
Zelditch, M. L. (2001) · Cited by 171
Adaptation, Versatility, and Evolution
Vermeij, G. J. (1973) · Systematic Zoology · doi:10.2307/2412953 · Cited by 169
GENETICS OF FLUCTUATING ASYMMETRY: A DEVELOPMENTAL MODEL OF DEVELOPMENTAL INSTABILITY
Klingenberg, C. P., & Nijhout, H. F. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb03772.x · Cited by 167
MORPHOLOGICAL INTEGRATION IN THE CARNIVORAN SKULL
Goswami, A. (2006) · Evolution · doi:10.1111/j.0014-3820.2006.tb01091.x · Cited by 163
Self-citationBastir, M., & Rosas, A. (2006) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2006.03.009 · Cited by 152
Duplication of Modules Facilitates the Evolution of Functional Specialization
Calabretta, R., Nolfi, S., Parisi, D., & Wagner, G. P. (2000) · Artificial Life · doi:10.1162/106454600568320 · Cited by 141
ONTOGENETIC VARIATION IN PATTERNS OF PHENOTYPIC INTEGRATION IN THE LABORATORY RAT
Zelditch, M. L. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb04105.x · Cited by 141
Craniofacial variability and modularity in macaques and mice
Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. L. (2004) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21002 · Cited by 134
The Evolutionary Value of Recombination Is Constrained by Genome Modularity
Martin, D. P., van der Walt, E., Posada, D., & Rybicki, E. P. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010051 · Cited by 122
In Search of the Biological Significance of Modular Structures in Protein Networks
Wang, Z., & Zhang, J. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030107 · Cited by 118
Zelditch, M. L., & Carmichael, C. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb05179.x · Cited by 114
Cheverud, J. M., Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., & Pletscher, L. S. (2004) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21008 · Cited by 112
Sears, K. E., Goswami, A., Flynn, J. J., & Niswander, L. A. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00196.x · Cited by 106
Self-citationA COMPARATIVE ANALYSIS OF MORPHOLOGICAL VARIATION PATTERNS IN THE PAPIONINS
Cheverud, J. M. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb02623.x · Cited by 101
Integration, phylogeny, and the hominid cranial base
Strait, D. S. (2001) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1041 · Cited by 100
Cheverud, J. M., Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., & Pletscher, L. S. (2004) · Journal of Experimental Zoology · doi:10.1002/jez.21008 · Cited by 100
Van Der Klaauw, C. J. (1952) · Archives Néerlandaises de Zoologie · doi:10.1163/187530152x00017 · Cited by 96
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
Integration, Modules, and Development: Molecules to Morphology to Evolution
Klingenberg, C. P. (2004) · Oxford University Press eBooks · doi:10.1093/oso/9780195160437.003.0010 · Cited by 82
Marroig, G., de Vivo, M., & Cheverud, J. M. (2004) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2003.00653.x · Cited by 81
Bruner, E., & Ripani, M. (2008) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20837 · Cited by 79
Adaptation and the modular design of organisms
Wagner, G. P. (1995) · Lecture notes in computer science · doi:10.1007/3-540-59496-5_308 · Cited by 75
Brief communication: Cutmarks on a Plio-Pleistocene hominid from Sterkfontein, South Africa
Pickering, T. R., White, T. D., & Toth, N. P. (2000) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(200004)111:4 · Cited by 71
Morphological Integration Primate Evolution
Ackermann, R., & Cheverud, J. M. (2004) · doi:10.1093/oso/9780195160437.003.0014 · Cited by 57
Agutter, P. S., & Wheatley, D. N. (2000) · BioEssays · doi:10.1002/1521-1878(200011)22:11 · Cited by 56
The Macroevolution of Phenotypic Integration
Eble, G. J. (2004) · Oxford University Press eBooks · doi:10.1093/oso/9780195160437.003.0012 · Cited by 48
Growth and Intensity of Integration through Postnatal Growth in the Skull of Sigmodon fulviventer
Zelditch, M. L., & Carmichael, A. C. (1989) · Journal of Mammalogy · doi:10.2307/1381419 · Cited by 47
Marroig, G., & Cheverud, J. M. (2004) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10421 · Cited by 46
Phylogeny, Diet, and Cranial Integration in Australodelphian Marsupials
Goswami, A. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000995 · Cited by 42
Self-citationArchives néerlandaises de zoologie
Vereniging, K. N. D. (1967) · Cited by 29
The correlated evolution of Runx2 tandem repeats and facial length in Carnivora
Sears, K. E., Goswami, A., Flynn, J., & Niswander, L. A. (2007) · UCL Discovery (University College London) · Cited by 6
Self-citationThe evolutionary value of recombination is constrained by genome modularity
Martin, D. P., van der Walt, E., Posada, D., & Rybicki, E. P. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010051.eor · Cited by 6
Flagged first, then by citations
Research works printed but not linked: 7
- [4]Schlosser G Wagner GP 2004 Modularity in development and evolution. Chicago University of Chicago Press 1 600
- [6]Atchley WR 1993 Genetic and developmental aspects of variability in the mammalian mandible. Hanken J Hall BK The Skull Chicago University of Chicago Press 207 247
- [27]Zelditch ML Moscarella RA 2004 Form, function and life history: spatial and temporal dynamics of integration. Pigliucci M Preston K Phenotypic Integration Oxford Oxford University Press 274 301
- [36]Chernoff B Magwene PM 1999 Afterword. Olson EC Miller RL Morphological Integration Chicago University of Chicago Press 319 348
- [42]Shubin N Davis MC 2004 Modularity in the evolution of vertebrate appendages. Schlosser G Wagner GP Modularity in development and evolution Chicago University of Chicago Press 429 440
- [54]Rose K Archibald D 2005 The rise of placental mammals: origins and relaitonships of the major extant clades. Baltimore Johns Hopkins University Press 259
- [59]Cheverud JM 1988 Spatial-Analysis in Morphology Illustrated by Rhesus Macaque Cranial Growth and Integration. American Journal of Physical Anthropology 75 195 196
Cited by
Sorted by citations
Evolution and development of shape: integrating quantitative approaches
Klingenberg, C. P. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2829 · Cited by 706
Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications
Klingenberg, C. P. (2015) · Symmetry · doi:10.3390/sym7020843 · Cited by 456
Studying morphological integration and modularity at multiple levels: concepts and analysis
Klingenberg, C. P. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0249 · Cited by 381
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
Self-citationDevelopmental origins of mosaic evolution in the avian cranium
Felice, R. N., & Goswami, A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716437115 · Cited by 249
“A similar pattern has been demonstrated in the mammal cranium (14).”
BackgroundSelf-citation
Metadata
- Authors
- Goswami, A., & Polly, P. D.
- Affiliations
- University College London (GB)
- Indiana University Bloomington (US)
- Corresponding author
- Goswami, Anjali
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-03-03
- Volume
- 5
- Issue
- 3
- Pages
- e9517
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2831076
- OpenAlex
- W2073056334
- Cited by
- 271
- References
- 64
- Citations by year
- 2026: 14 · 2025: 14 · 2024: 10 · 2023: 16 · 2022: 12 · 2021: 25 · 2020: 45 · 2019: 32 · 2018: 19 · 2017: 17 · 2016: 11 · 2015: 15 · 2014: 13 · 2013: 9 · 2012: 5
- FWCI
- 10.66
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- National Science Foundation (0308765, 0502186)
- American Museum of Natural History
- University of Chicago
- Field Museum
- National Museum of Natural History
- Office of International Science and Engineering
- University of California Museum of Paleontology
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Morphological variations and asymmetry
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Health Sciences › Medicine › Anatomy › Comparative Animal Anatomy Studies
- Keywords
- modularity, skull morphology, morphological disparity, trait integration, developmental constraints, Carnivora, primates, placental mammals, skull base, macroevolution, skull evolution
- MeSH terms
- Animals, Carnivora, Biological Evolution, Female, Fossils, Male, Mammals, Models, Anatomic, Primates, Random Allocation, Skull
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