Ontogenetic integration of the hominoid face
Abstract
By investigating similarity in cranial covariation patterns, it is possible to locate underlying functional and developmental causes for the patterning, and to make inferences about the evolutionary forces that have acted to produce the patterns. Furthermore, establishing where these covariation patterns may diverge in ontogeny can offer insight into when selection may have acted on development. Here, covariation patterns are compared among adult and non-adult members of the African ape/human clade, in order to address three questions. First, are integration patterns constant among adult African apes and humans? Second, are they are constant in non-adults--i.e. throughout ontogeny? Third, if they are not constant, when do they diverge? Measurements are obtained from 677 crania of adult and non-adult African apes and humans. In order to address the first two questions, correlation matrices and theoretical integration matrices are compared using matrix correlation methods. The third question is evaluated by comparing correlation and variance/covariance patterns, using matrix correlation and random skewers methods, respectively, between adjacent age categories within each species, and between equivalent age categories among the four species. Results show that the hominoids share a similar pattern of ontogenetic integration, suggesting that common developmental/functional integrative processes may play an important role in keeping covariance structure stable across this lineage. However, there are some important differences in the magnitude of integration and in phenotypic covariance structure among the species, which may provide some insight into how selection acted to differentiate humans from the great apes.
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?
Patterns of covariation and correlation between different parts of the cranium are partially independent, suggesting they behave as partially independent units.
“In fact, different studies have shown that the patterns of covariation and correlation between different parts of the cranium are partially independent, thus suggesting that they behave as partially independent units [15,39–42].”
From Morphological consequences of artificial cranial deformation: Modularity and integration (2020) · cites this paper as [40]
Facial growth is closely integrated with the development of the braincase and other cranial components, highlighting interdependence of morphological modules during growth and development.
“facial growth is closely integrated with the development of the braincase (neurocranium), and other cranial components 4 , highlighting the interdependence of different morphological traits, or modules, during growth and development 5,6”
From The evolutionary history of the human face (2019) · cites this paper as [5]
Cites
An Introduction to the Bootstrap
Efron, B., & Tibshirani, R. J. (1994) · doi:10.1201/9780429246593 · Cited by 40,500 · see citing works
Developmental Plasticity and Evolution
West-Eberhard, M. J. (2003) · doi:10.1093/oso/9780195122343.001.0001 · Cited by 6,115 · see citing works
The measurement of selection on correlated characters
Lande, R., & Arnold, S. J. (1983) · Evolution · doi:10.1111/j.1558-5646.1983.tb00236.x · Cited by 5,437 · see citing works
The Apportionment of Human Diversity
Lewontin, R. C. (1972) · Evolutionary Biology · doi:10.1007/978-1-4684-9063-3_14 · Cited by 2,472 · see citing works
Multiple Regression and Correlation Extensions of the Mantel Test of Matrix Correspondence
Smouse, P. E., Long, J. C., & Sokal, R. R. (1986) · Systematic Zoology · doi:10.2307/2413122 · Cited by 2,216 · see citing works
Evolutionary quantitative genetics
(1998) · Choice Reviews Online · doi:10.5860/choice.35-5054 · Cited by 1,307 · see citing works
Primate adaptation and evolution
(1989) · Choice Reviews Online · doi:10.5860/choice.26-3889 · Cited by 1,246 · see citing works
A Quantitative Genetic Theory of Life History Evolution
Lande, R. (1982) · Ecology · doi:10.2307/1936778 · Cited by 1,097 · 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
Phenotypic integration: studying the ecology and evolution of complex phenotypes
Pigliucci, M. (2003) · Ecology Letters · doi:10.1046/j.1461-0248.2003.00428.x · Cited by 815 · see citing works
Shape, relative size, and size-adjustments in morphometrics
Jungers, W. L., Falsetti, A. B., & Wall, C. E. (1995) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330380608 · Cited by 759 · see citing works
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 750 · see citing works
Heterochrony and allometry: the analysis of evolutionary change in ontogeny
Klingenberg, C. P. (1998) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s000632319800512x · Cited by 712 · see citing works
Comparison of cranial ontogenetic trajectories among great apes and humans
Mitterœcker, P., Gunz, P., Bernhard, M., Schæfer, K., & Bookstein, F. L. (2004) · Journal of Human Evolution · doi:10.1016/j.jhevol.2004.03.006 · Cited by 601 · 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
An apportionment of human DNA diversity
Barbujani, G., Magagni, A., Minch, E., & Cavalli-Sforza, L. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.9.4516 · Cited by 498 · see citing works
Australopithecus garhi : A New Species of Early Hominid from Ethiopia
Asfaw, B., White, T. D., Lovejoy, O., Latimer, B., Simpson, S. W., & Suwa, G. (1999) · Science · doi:10.1126/science.284.5414.629 · Cited by 495 · see citing works
Canonical and principal components of shape
Darroch, J. N., & Mosimann, J. E. (1985) · Biometrika · doi:10.1093/biomet/72.2.241 · Cited by 490 · see citing works
The Nariokotome Homo Erectus Skeleton
(1993) · Springer eBooks · doi:10.1007/978-3-662-10382-1 · Cited by 483 · see citing works
THE MAXIMUM F-RATIO AS A SHORT-CUT TEST FOR HETEROGENEITY OP VARIANCE
Hartley, H. O. (1950) · Biometrika · doi:10.1093/biomet/37.3-4.308 · Cited by 443 · 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
Myosin gene mutation correlates with anatomical changes in the human lineage
Stedman, H. H., Kozyak, B. W., Nelson, A., Thesier, D. M., Su, L. T., Low, D. W., Bridges, C. R., Shrager, J. B., Minugh-Purvis, N., & Mitchell, M. A. (2004) · Nature · doi:10.1038/nature02358 · 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
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
A reappraisal of early hominid phylogeny
Strait, D. S., Grine, F. E., & Moniz, M. A. (1997) · Journal of Human Evolution · doi:10.1006/jhev.1996.0097 · Cited by 330 · see citing works
Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets
Ruvolo, M. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025761 · Cited by 328 · see citing works
Neanderthal cranial ontogeny and its implications for late hominid diversity
de León, M. S. P., & Zollikofer, C. P. E. (2001) · Nature · doi:10.1038/35087573 · Cited by 321 · see citing works
DENTAL DEVELOPMENT AS A MEASURE OF LIFE HISTORY IN PRIMATES
Smith, B. H. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb04266.x · Cited by 320 · see citing works
Cheverud, J. M., Rutledge, J. J., & Atchley, W. R. (1983) · Evolution · doi:10.1111/j.1558-5646.1983.tb05619.x · Cited by 297 · see citing works
Methods for the Comparative Analysis of Variation Patterns
Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989) · Systematic Zoology · doi:10.2307/2992282 · Cited by 296 · see citing works
Viðarsdóttir, U. S., O'Higgins, P., & Stringer, C. (2002) · Journal of Anatomy · doi:10.1046/j.1469-7580.2002.00092.x · Cited by 274 · see citing works
Cheverud, J. M. (1996) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1996.9010005.x · Cited by 222 · see citing works
Probabilities of Non-Positive Definite between-Group or Genetic Covariance Matrices
Hill, W. G., & Thompson, R. (1978) · Biometrics · doi:10.2307/2530605 · Cited by 213 · see citing works
Modification of Estimates of Parameters in the Construction of Genetic Selection Indices ('Bending')
Hayes, J. F., & Hill, W. G. (1981) · Biometrics · doi:10.2307/2530561 · Cited by 199 · see citing works
Morphological analysis of the mammalian postcranium: A developmental perspective
Lovejoy, C. O., Cohn, M. J., & White, T. D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13247 · Cited by 187 · see citing works
Evolutionary relationships among early hominids
Skelton, R. R., & McHenry, H. M. (1992) · Journal of Human Evolution · doi:10.1016/0047-2484(92)90070-p · Cited by 168 · see citing works
Miocene Fossil Hominids and the Chimp-Human Clade
Begun, D. R. (1992) · Science · doi:10.1126/science.1411507 · Cited by 166 · see citing works
Ecological Genetics: The Interface
Brussard, P. F. (1978) · Proceedings in life sciences · doi:10.1007/978-1-4612-6330-2 · Cited by 158 · see citing works
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 · see citing works
González‐José, R., der Molen, S. V., González‐Pérez, E., & Hernández, M. (2003) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10302 · Cited by 132 · see citing works
The Robust Australopithecine Face: A Morphogenetic Perspective
McCollum, M. A. (1999) · Science · doi:10.1126/science.284.5412.301 · Cited by 125 · see citing works
Phylogenetic Analysis of Early Hominids [and Comments and Reply]
Skelton, R. R., McHenry, H. M., Drawhorn, G. M., et al. (1986) · Current Anthropology · doi:10.1086/203377 · Cited by 117 · see citing works
Zelditch, M. L., & Carmichael, C. (1989) · Evolution · doi:10.1111/j.1558-5646.1989.tb05179.x · Cited by 114 · see citing works
Common patterns of facial ontogeny in the hominid lineage
Ackermann, R., & Krovitz, G. E. (2002) · The Anatomical Record · doi:10.1002/ar.10119 · Cited by 112 · see citing works
Self-citationAckermann, R. (2002) · Journal of Human Evolution · doi:10.1006/jhev.2002.0569 · Cited by 105 · see citing works
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 · see citing works
Integration, phylogeny, and the hominid cranial base
Strait, D. S. (2001) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1041 · Cited by 100 · see citing works
Cheverud, J. M., & Dow, M. M. (1985) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330670206 · Cited by 95 · see citing works
Rosas, A., & Bastir, M. (2004) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20049 · Cited by 93 · see citing works
O’Higgins, P., Chadfield, P., & Jones, N. (2001) · Journal of Zoology · doi:10.1017/s095283690100084x · Cited by 86 · see citing works
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 · see citing works
Subnasal morphological variation in extant hominoids and fossil hominids
McCollum, M. A., Grine, F. E., Ward, S., et al. (1993) · Journal of Human Evolution · doi:10.1006/jhev.1993.1009 · Cited by 58 · see citing works
Morphological Integration Primate Evolution
Ackermann, R., & Cheverud, J. M. (2004) · doi:10.1093/oso/9780195160437.003.0014 · Cited by 57 · see citing works
Self-citationPopulation Differentiation: Something New or More of the Same?
Sokal, R. R. (1978) · Proceedings in life sciences · doi:10.1007/978-1-4612-6330-2_12 · 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
COMPARISON OF QUANTITATIVE GENETIC PARAMETERS
Cowley, D. E., & Atchley, W. R. (1992) · Evolution · doi:10.1111/j.1558-5646.1992.tb01184.x · Cited by 35 · see citing works
A Morphometric Study of Facial Growth
Richtsmeier, J. T., & Walker, A. (1993) · Springer eBooks · doi:10.1007/978-3-662-10382-1_16 · Cited by 29 · see citing works
Trait list bias? A reply to Skelton and McHenry
Strait, D. S., & Grine, F. E. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1997.0196 · Cited by 28 · see citing works
Krovitz, G. E. (2000) · Medical Entomology and Zoology · Cited by 20 · see citing works
Using extant morphological variation to understand fossil relationships: a cautionary tale
Ackermann, R. (2003) · Open University of Cape Town (University of Cape Town) · Cited by 17 · see citing works
Self-citationAckermann, R. (1999) · Medical Entomology and Zoology · Cited by 12 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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
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
Epigenetic 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
Singh, N., Harvati, K., Hublin, J.-J., & Klingenberg, C. P. (2012) · Journal of Human Evolution · doi:10.1016/j.jhevol.2011.11.006 · Cited by 129 · see citing works
Speculations about the selective basis for modern human craniofacial form
Lieberman, D. E. (2008) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20154 · Cited by 109 · see citing works
The evolutionary history of the human face
Lacruz, R. S., Stringer, C. B., Kimbel, W. H., Wood, B., Harvati, K., O’Higgins, P., Bromage, T. G., & Arsuaga, J.-L. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0865-7 · Cited by 108 · see citing works
Bruner, E., & Ripani, M. (2008) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20837 · Cited by 79 · see citing works
Pearson, O. M. (2008) · Evolutionary Anthropology: Issues, News, and Reviews · doi:10.1002/evan.20155 · Cited by 73 · see citing works
The contribution of subsistence to global human cranial variation
Noback, M. L., & Harvati, K. (2015) · Journal of Human Evolution · doi:10.1016/j.jhevol.2014.11.005 · Cited by 66 · see citing works
Patterns of craniofacial integration in extantHomo,Pan, andGorilla
Polanski, J. M., & Franciscus, R. G. (2006) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20421 · Cited by 54 · see citing works
Allometric scaling of infraorbital surface topography in Homo
Maddux, S. D., & Franciscus, R. G. (2009) · Journal of Human Evolution · doi:10.1016/j.jhevol.2008.10.003 · Cited by 51 · 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
The facial skeleton of the chimpanzee‐human last common ancestor
Cobb, S. N. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00866.x · Cited by 20 · see citing works
Villmoare, B. A., Dunmore, C., Kilpatrick, S., Oertelt, N., Depew, M. J., & Fish, J. L. (2014) · Journal of Human Evolution · doi:10.1016/j.jhevol.2014.06.014 · Cited by 16 · see citing works
Cottin, M., Khonsari, R. H., & Friess, M. (2017) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2017.03.001 · Cited by 9 · see citing works
Modularidad e integración morfológica en cráneos humanos: un enfoque morfométrico geométrico
Püschel, T. (2014) · International Journal of Morphology · doi:10.4067/s0717-95022014000100048 · Cited by 8 · see citing works
- Authors
- ACKERMANN, R.
- Affiliations
- University of Cape Town (ZA)
- Corresponding author
- ACKERMANN, R
- ORCID
- ACKERMANN, R
- Venue
- Journal of Human Evolution
- Publisher
- Elsevier BV
- Published
- 2005-02
- Volume
- 48
- Issue
- 2
- Pages
- 175-197
- ISSN
- 0047-2484 (ISSN-L)
- OpenAlex
- W2014292567
- Cited by
- 150
- References
- 62
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2021: 3 · 2020: 4 · 2019: 18 · 2018: 10 · 2017: 10 · 2016: 6 · 2015: 4 · 2014: 13 · 2013: 15 · 2012: 8
- FWCI
- 10.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Human Evolution (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Arts and Humanities › Archeology › Forensic Anthropology and Bioarchaeology Studies
- Keywords
- cranial integration, developmental constraints, human evolution, great apes, skull morphology, covariance structure, age-related variation
- MeSH terms
- Adolescent, Adult, Africa, Animals, Child, Biological Evolution, Face, Fossils, Humans, Skull, Hominidae
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