Ontogenetic Allometry and Cranial Shape Diversification Among Human Populations From South America

Modifications of ontogenetic allometries play an important role in patterning the shape differentiation among populations. This study evaluates the influence of size variation on craniofacial shape disparity among human populations from South America and assesses whether the morphological disparity observed at the interpopulation level resulted from a variable extension of the same ontogenetic allometry, or whether it arose as a result of divergences in the pattern of size‐related shape changes. The size and shape of 282 adult and subadult crania were described by geometric morphometric‐based techniques. Multivariate regressions were used to evaluate the influence of size on shape differentiation between and within populations, and phylogenetic comparative methods were used to take into account the shared evolutionary history among populations. The phylogenetic generalized least‐squares models showed that size accounts for a significant amount of shape variation among populations for the vault and face but not for the base, suggesting that the three modules did not exhibit a uniform response to changes in overall growth. The common slope test indicated that patterns of evolutionary and ontogenetic allometry for the vault and face were similar and characterized by a heightening of the face and a lengthening of the vault with increasing size. The conservation of the same pattern of shape changes with size suggests that differences in the extent of growth contributed to the interpopulation cranial shape variation and that certain directions of morphological change were favored by the trait covariation along ontogeny. Anat Rec, 2011. © 2011 Wiley‐Liss, Inc.

[1]  James Steele,et al.  AMS 14C dating of early human occupation of southern South America , 2009 .

[2]  Eric J. Schmidt,et al.  Rediscovering Waddington in the post‐genomic age , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[3]  R. Cousin [Craniofacial development]. , 1979, Bulletin de l'Academie de chirurgie dentaire.

[4]  Douglas J Emlen,et al.  Size and shape: the developmental regulation of static allometry in insects , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[5]  C. Klingenberg Developmental constraints, modules, and evolvability , 2005 .

[6]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[7]  A. Gustafsson,et al.  Human size evolution: no evolutionary allometric relationship between male and female stature. , 2004, Journal of human evolution.

[8]  M. Aguiar,et al.  Searching for Modular Structure in Complex Phenotypes: Inferences from Network Theory , 2009, Evolutionary Biology.

[9]  Peter Dangerfield,et al.  Developmental Juvenile Osteology. By LOUISE SCHEUER and SUE BLACK. (Pp. x+587; fully illustrated; $159 hardback; ISBN 0 12 624000 0.) San Diego: Academic Press. 2000 , 2001 .

[10]  S. Gould ALLOMETRY AND SIZE IN ONTOGENY AND PHYLOGENY , 1966, Biological reviews of the Cambridge Philosophical Society.

[11]  A Cherryson,et al.  Human Skeletal Remains , 2000 .

[12]  Trish E. Parsons,et al.  Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation , 2009, Evolutionary Biology.

[13]  H. Nijhout,et al.  The control of growth , 2003, Development.

[14]  J. Cheverud,et al.  Detecting genetic drift versus selection in human evolution , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  F. Bookstein,et al.  Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes , 2005, Evolution & development.

[16]  L. Humphrey,et al.  Growth patterns in the modern human skeleton. , 1998, American journal of physical anthropology.

[17]  Christian Peter Klingenberg,et al.  MULTIVARIATE ALLOMETRY , 2007 .

[18]  G. Eble,et al.  Allometric Space and Allometric Disparity: A Developmental Perspective in the Macroevolutionary Analysis of Morphological Disparity , 2008, Evolution; international journal of organic evolution.

[19]  H David Sheets,et al.  Comparison of geometric morphometric outline methods in the discrimination of age-related differences in feather shape , 2006, Frontiers in Zoology.

[20]  D. L. Swiderski SEPARATING SIZE FROM ALLOMETRY: ANALYSIS OF LOWER JAW MORPHOLOGY IN THE FOX SQUIRREL, SCIURUS NIGER , 2003 .

[21]  J. Cheverud,et al.  A COMPARISON OF PHENOTYPIC VARIATION AND COVARIATION PATTERNS AND THE ROLE OF PHYLOGENY, ECOLOGY, AND ONTOGENY DURING CRANIAL EVOLUTION OF NEW WORLD MONKEYS , 2001, Evolution; international journal of organic evolution.

[22]  P. O'higgins,et al.  A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton † , 2002, Journal of anatomy.

[23]  C. Hall,et al.  Developmental Juvenile Osteology , 2000 .

[24]  T. Goebel,et al.  The Late Pleistocene Dispersal of Modern Humans in the Americas , 2008, Science.

[25]  V. Bernal,et al.  Differences between sliding semi‐landmark methods in geometric morphometrics, with an application to human craniofacial and dental variation , 2006, Journal of anatomy.

[26]  B. Hallgrímsson,et al.  Evolvability as the proper focus of evolutionary developmental biology , 2007, Evolution & development.

[27]  G. Marroig When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini) , 2007, BMC Evolutionary Biology.

[28]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[29]  F. Bookstein,et al.  Morphometric Tools for Landmark Data: Geometry and Biology , 1999 .

[30]  R. Thorington,et al.  POSTNATAL ONTOGENY OF MARMOT (RODENTIA, SCIURIDAE) CRANIA: ALLOMETRIC TRAJECTORIES AND SPECIES DIVERGENCE , 2006 .

[31]  Fred L. Bookstein,et al.  Corpus Callosum Shape and Neuropsychological Deficits in Adult Males with Heavy Fetal Alcohol Exposure , 2002, NeuroImage.

[32]  J. Cheverud PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM , 1982, Evolution; international journal of organic evolution.

[33]  F J Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[34]  M. Depew,et al.  19 – Craniofacial Development , 2002 .

[35]  C. Klingenberg Heterochrony and allometry: the analysis of evolutionary change in ontogeny , 1998, Biological reviews of the Cambridge Philosophical Society.

[36]  J. Diniz‐Filho,et al.  Ecological and evolutionary factors in dental morphological diversification among modern human populations from southern South America , 2010, Proceedings of the Royal Society B: Biological Sciences.

[37]  S. Bamforth,et al.  Development and tissue origins of the mammalian cranial base. , 2008, Developmental biology.

[38]  P. Brakefield,et al.  Natural Selection and Developmental Constraints in the Evolution of Allometries , 2005, Science.

[39]  F. Bookstein,et al.  The Evolutionary Role of Modularity and Integration in the Hominoid Cranium , 2008, Evolution; international journal of organic evolution.

[40]  B. Hallgrímsson,et al.  Mouse models and the evolutionary developmental biology of the skull. , 2008, Integrative and comparative biology.

[41]  G. Holloway,et al.  Phenotypic Plasticity: Beyond Nature and Nurture , 2002, Heredity.

[42]  D. Adams,et al.  Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae) , 2010, BMC Evolutionary Biology.

[43]  P. O'higgins,et al.  Hominins do not share a common postnatal facial ontogenetic shape trajectory. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[44]  F. Bookstein,et al.  Comparison of cranial ontogenetic trajectories among great apes and humans. , 2004, Journal of human evolution.

[45]  C. Klingenberg There's something afoot in the evolution of ontogenies , 2010, BMC Evolutionary Biology.

[46]  Christian Peter Klingenberg,et al.  The pace of morphological change: historical transformation of skull shape in St Bernard dogs , 2008, Proceedings of the Royal Society B: Biological Sciences.

[47]  V. Bernal,et al.  The role of diet and temperature in shaping cranial diversification of South American human populations: an approach based on spatial regression and divergence rate tests , 2011 .

[48]  R. Lande QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY , 1979, Evolution; international journal of organic evolution.

[49]  S. I. Perez,et al.  Nonrandom Factors in Modern Human Morphological Diversification: A Study of Craniofacial Variation in Southern South American Populations , 2009, Evolution; international journal of organic evolution.

[50]  SPATIOTEMPORAL REORGANIZATION OF GROWTH RATES IN THE EVOLUTION OF ONTOGENY , 2000, Evolution; international journal of organic evolution.

[51]  Valeria Bernal,et al.  Variation and causal factors of craniofacial robusticity in Patagonian hunter‐gatherers from the late Holocene , 2006, American journal of human biology : the official journal of the Human Biology Council.

[52]  Owl,et al.  New World Monkeys , 2013 .

[53]  M. Sánchez-Villagra,et al.  Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents , 2010, Proceedings of the Royal Society B: Biological Sciences.

[54]  Valeria Bernal,et al.  Morphological differentiation of aboriginal human populations from Tierra del Fuego (Patagonia): implications for South American peopling. , 2007, American journal of physical anthropology.

[55]  Gillian M. Morriss‐Kay,et al.  Derivation of the mammalian skull vault , 2001, Journal of anatomy.

[56]  V. Bernal,et al.  Ontogeny of robusticity of craniofacial traits in modern humans: a study of South American populations. , 2009, American journal of physical anthropology.