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Cited by 271Morphological variations and asymmetryEvolution and Paleontology StudiesComparative Animal Anatomy Studies

The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)

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Goswami, Anjali, Polly, P. David·2010·PLoS ONE
DOI 10.1371/journal.pone.0009517PMC PMC2831076
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Abstract

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 of high integration associated with low evolutionary rates and low disparity has been demonstrated in the mammal cranium.

    “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]

    The Principal Findings report low disparity in the highly integrated primate cranial base, and the Discussion says significant results tended to support integration constraining morphological evolution. But 14 of 24 disparity results were not significant, an integrated molar module had high disparity, and the study measured disparity rather than evolutionary rates. The claim presents a qualified finding as a general pattern and adds a low-rate finding the paper does not demonstrate. (LLM, conf=0.88)

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Research works printed but not linked: 7

  1. [4]Schlosser G Wagner GP 2004 Modularity in development and evolution. Chicago University of Chicago Press 1 600
  2. [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
  3. [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
  4. [36]Chernoff B Magwene PM 1999 Afterword. Olson EC Miller RL Morphological Integration Chicago University of Chicago Press 319 348
  5. [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
  6. [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
  7. [59]Cheverud JM 1988 Spatial-Analysis in Morphology Illustrated by Rhesus Macaque Cranial Growth and Integration. American Journal of Physical Anthropology 75 195 196

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Authors
Goswami, A., & Polly, P. D.
Affiliations
  • University College London (GB)
  • Indiana University Bloomington (US)
Corresponding author
Goswami, Anjali
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2010-03-03
Volume
5
Issue
3
Pages
e9517
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0009517
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
Licence
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
  • Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Health Sciences › Medicine › Urology › 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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