The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“A similar pattern has been demonstrated in the mammal cranium (14).”
From Developmental origins of mosaic evolution in the avian cranium (2018) · cites this paper as [14]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
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
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
Items 201–271 of 271
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · doi:10.1017/9781316591383.001 · Cited by 1
Kelly, E. M. (2011) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Morphology and Evolution of the Ceratopsian Skull
Knapp, A. (2020) · Queen Mary Research Online (Queen Mary University of London)
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.013
The Pelvic Girdle and Hindlimb Skeleton
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.010
Primate Development and Growth
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.004
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.007
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.008
Quantitative Approaches to Phylogenetics
Folinsbee, K. E., Evans, D. C., Fröbisch, J., Brooks, D. R., & Tsuji, L. A. (2014) · Springer eBooks · doi:10.1007/978-3-642-39979-4_5
Functional Morphology of the Pelvis
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.004
Developmental Biology of the Pelvis
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.006
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · doi:10.1017/9781316591383.002
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.003
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.003
Quantitative Approaches to Phylogenetics
Folinsbee, K. E., Evans, D. C., Fröbisch, J., Brooks, D. R., & Tsuji, L. A. (2013) · Springer eBooks · doi:10.1007/978-3-642-27800-6_5-6
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.001
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.002
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.014
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.012
Morphological Integration, Evolutionary Processes and Variation in the Human Pelvis
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.007
(2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.010
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.009
The Newborn Primate Body Form: Phylogenetic and Life-History Influences
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.011
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.005
EVOLVABILITY IN THE FOSSIL RECORD
Institution, S., Hunt, G., Love, A. C., Grabowski, M. W., Houle, D., Liow, L. H., Porto, A., Tsuboi, M., & Voje, K. L. (2021) · Abstracts with programs - Geological Society of America · doi:10.1130/abs/2021am-369056
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · Cambridge University Press eBooks · doi:10.1017/9781316591383.015
Smith, T. D., DeLeon, V. B., Vinyard, C. J., & Young, J. W. (2020) · doi:10.1017/9781316591383.016
Wall‐Scheffler, C. M., Kurki, H. K., & Auerbach, B. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108185738.011
Biosocial complexity and the skull
White, S., & Menéndez, L. P. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821383-4.00008-5
A Putative Locus for Cranial-Size Variability of the Fox (Vulpes vulpes)
Kharlamova, A. V., Шихевич, С. Г., Vladimirova, A. V., Kukekova, A. V., & Efimov, V. M. (2023) · Russian Journal of Genetics · doi:10.1134/s1022795423050083
Putative Locus for Cranial Size Variability of the Fox (Vulpes vulpes)
Kharlamova, A. V., Шихевич, С. Г., Vladimirova, A. V., Kukekova, A. V., & Efimov, V. M. (2023) · Генетика · doi:10.31857/s0016675823050089
Evaluating the Evolvability of Paranthropus Cranial Morphology in Relation to Feeding Biomechanics
Jung, H., Rolian, C., Strait, D. S., & Baab, K. L. (2025) · American Journal of Biological Anthropology · doi:10.1002/ajpa.70136
Arlegi, M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.04.692052
Hopkins, M. J., Nikolic, M. C., Holmes, J. D., Monti, D., Vargas-Parra, E. E., Bicknell, R. D. C., Edgecombe, G. D., Jordan-Burmeister, K., Paterson, J. R., & Srivastava, S. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1002/brv.70183 · Cited by 2
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655634
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655637
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655643
Conith, A. J., Kidd, M. R., Kocher, T. D., & Albertson, R. C. (2020) · Figshare · doi:10.6084/m9.figshare.12750411
Rovinsky, D., Evans, A. R., & Adams, J. W. (2021) · Figshare · doi:10.6084/m9.figshare.14462700
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655649
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655646
Hanot, P., Bayarsaikhan, J., Guintard, C., Haruda, A. F., Mijiddorj, E., Schafberg, R., & Taylor, W. (2021) · Figshare · doi:10.6084/m9.figshare.16655640
Conith, A. J., Kidd, M. R., Kocher, T. D., & Albertson, R. C. (2020) · Figshare · doi:10.6084/m9.figshare.12750405
Allometry and ecology shape cranial variation in phyllotine gerbil mice (Eligmodontia)
Alhajeri, B. H. (2026) · Zoologischer Anzeiger · doi:10.1016/j.jcz.2026.01.001
Mironovsky, A. N., Кожара, А. В., & Slynko, E. E. (2025) · Biology Bulletin · doi:10.1134/s1062359025700736
Arlegui, M. (2019) · theses.fr (ABES) · doi:10.70675/fe618e4dzcc79z4469zb6edz14c263ede1fa
Impact of ecological strategies on the morphological rate, diversity and integration in Carnivora
Michaud, M. (2019) · theses.fr (ABES) · doi:10.70675/adaa5031z7360z469aza36az77efc92b13db
Morphological integration of the avian beak facilitates evolution along lines of least resistancePreprint
Ely, R., Sommer, S., & Hipsley, C. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.04.722668
Kovaleva, V. Y., Efimov, V. M., Moroldoev, I. V., & Litvinov, Y. N. (2026) · Russian Journal of Theriology · doi:10.15298/rusjtheriol.25.1.05
Structural Equation Modeling Reveals How Allometry Shapes Integration in Avian Cranial Evolution
Oyston, J. W., Thorson, J. T., Knapp, A., Marek, R. D., & Felice, R. N. (2026) · Integrative and Comparative Biology · doi:10.1093/icb/icag106
Fedorchuk, O. A. (2026) · American Journal of Biological Anthropology · doi:10.1002/ajpa.70313
Banerjee, R., & Venkatramana, P. (2026) · American Journal of Biological Anthropology · doi:10.1002/ajpa.70372
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
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