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Canalization, developmental stability, and morphological integration in primate limbs

Bibliographic Data

ID8317452
AuthorsBenedikt Hallgr msson, Benedikt Hallgr�msson (University of Calgary), Katherine E Willmore (0000-0002-8563-3354, University of Calgary), Katherine Willmore, Brian K Hall (0000-0003-4469-8300, Dalhousie University)
Year2002
Volume119
IssueS35
Pages131-158
Publication date2002-12-01
Peer ReviewedYes
Open AccessYes
TypeARTICLE
VenueAmerican Journal of Physical Anthropology (JOURNAL)
Journal identifiersISSN: 0002-9483 • E-ISSN: 1096-8644
PublisherWiley (PUBLISHER • GB)
DOI10.1002/ajpa.10182
PMID12653311
OpenAlexW2010655791
LanguageEN
Citations received71
References cited160

Canalization and developmental stability refer to the tendency of developmental processes to follow particular trajectories, despite external or internal perturbation. Canalization is the tendency for development of a specific genotype to follow the same trajectory under different conditions (different environments or different genetic backgrounds), while developmental stability is the tendency for the development of a specific genotype to follow the same trajectory under the same conditions. Morphological integration refers to the tendency for structures to show correlated variation because they develop in response to shared developmental processes or function in concert with other structures. All three phenomena are emergent properties of developmental systems that can affect the interaction of development and evolution. In this paper, we review the topics of canalization, developmental stability, and morphological integration and their relevance to primate and human evolution. We then test three developmentally motivated hypotheses about the patterning of variability components in the mammalian limb. We find that environmental variances and fluctuating asymmetries (FA) increase distally along the limb in adult macaques but not in fetal mice. We infer that the greater variability of more distal segments in macaques is due to postnatal mechanical effects. We also find that heritability and FA are significantly correlated when different limb measurements are compared in fetal mice. This supports the idea that the mechanisms underlying canalization and developmental stability are related. Finally, we report that the covariation structure of fore- and hindlimb skeletal elements shows evidence for morphological integration between serially homologous structures between the limbs. This is evidence for the existence of developmental modules that link structures between the limbs. Such modules would produce covariation that would need to be overcome by selection for divergence in hind- and forelimb morphology

Biology · Developmental psychology · Evolutionary biology · Fluctuating asymmetry · Gene · Heritability · Limb development · Primate · Anatomy · Genetics · Hemispheric Asymmetry in Neuroscience · Morphological variations and asymmetry · Neuroscience · Psychology

  • Cambio secular de la estatura de poblaciones de la Cuenca de México en la época prehispánica

    Open Access•Jonathan Mauricio Pérez Durán, Guillermo Rodríguez Tlachi et al.•Anales de Antropología•2023

  • Ontogenetic integration of the hominoid face

    Open Access•Rebecca Rogers Ackermann, R Ackermann•Journal of Human Evolution•2005

  • The Evolutionary Biology of the Human Pelvis

    Open Access•C M Wall-Scheffler, Helen Kurki et al.•Evolutionary Biology of the Human…•2019

  • The Ontogeny–Phylogeny Nexus in a Nutshell

    Peter R Menke•Handbook of paleoanthropology•2007

  • The Ontogeny-Phylogeny Nexus in a Nutshell

    Open Access•Peter R Menke•Handbook of Paleoanthropology•2013

  • The Ontogeny-Phylogeny Nexus in a Nutshell

    Open Access•Peter R Menke•Handbook of Paleoanthropology•2015

  • Having a Jolly Good Time-Together

    K M Wei•Current Anthropology•2009

  • Reconstructing Extinct Hominin Diets

    Frederick E Grine•Oxford Handbook of the…•2022

  • Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading

    Open Access•Timothy M Ryan, Colin N Shaw et al.•Proceedings of the National…•2015

  • Development and the evolvability of human limbs

    Open Access•Nicholas Maurice Young, Nathan M Young et al.•Proceedings of the National…•2010

  • Reconstructing the functional traits of the horses from the tomb of King Childeric

    Open Access•Pauline Hanot, Sylvain Gerber et al.•Journal of Archaeological Science•2020

  • Studying factors influencing facial developmental instability

    Open Access•Marie Jandová, Petra Urbanová•Annals of Human Biology•2021

  • Directional and fluctuating asymmetry among !Kung San and Kavango people of Northern Namibia

    Open Access•Kirchengast•American Journal of Human Biology•2017

  • Shifts in subsistence type and its impact on the human skull's morphological integration

    Open Access•Carolina Paschetta, Soledad De Azevedo et al.•American Journal of Human Biology•2016

  • Patterns of directional asymmetry in the pelvis and pelvic canal

    Open Access•Victoria A Tobolsky, Helen Kurki et al.•American Journal of Human Biology•2016

  • Brain size growth in wild and captive chimpanzees ( Pan troglodytes )

    Open Access•Z Cofran•American Journal of Primatology•2018

  • Heritability in the Rhesus Macaque ( Macaca mulatta ) Vertebral Column

    Open Access•Catalina I Villamil, Jeziel J Negrón et al.•American Journal of Primatology•2025

  • The befuddling nature of mouse lemur hands and feet at Bezà Mahafaly, SW Madagascar

    Open Access•Gina Agostini, Emilienne Rasoazanabary et al.•American Journal of Primatology•2017

  • Dental Fluctuating Asymmetry

    Open Access•L A P Kohn, Kurt Schulz et al.•American Journal of Primatology•2025

  • The enduring puzzle of the human chin

    Open Access•James D Pampush, David J Daegling•Evolutionary Anthropology Issues…•2016

  • Phonological potentials and the lower vocal tract

    Open Access•Scott R Moisik, Ewa Czaykowska-Higgins et al.•Journal of the International…•2021

  • The enigmatic relationship between epiphyseal fusion and bone development in primates

    Open Access•Conrad Stephen Brimacombe•Evolutionary Anthropology Issues…•2017

  • Genes, development, and evolvability in primate evolution

    Open Access•C Rolian•Evolutionary Anthropology Issues…•2014

  • Levels of Intraspecific Variation Within the Catarrhine Skeleton

    Open Access•L T Buck, Jay T Stock et al.•International Journal of…•2010

  • What Evolvability Really Is

    Rachael L Brown•The British Journal for the…•2014

  • Why are rare traits unilaterally expressed

    Open Access•Benedikt Hallgrimsson, Barra Ó Donnabháin et al.•American Journal of Physical…•2005

  • Who's afraid of the big bad Wolff

    Open Access•C B Ruff, Christopher Ruff et al.•American Journal of Physical…•2006

  • Epiphyseal fusion and dental development in Pan paniscus with comparisons with Pan troglodytes

    Open Access•Conrad Stephen Brimacombe, Kevin L Kuykendall et al.•American Journal of Physical…•2018

  • Trisomy 21 and facial developmental instability

    Open Access•John M Starbuck, Theodore M Cole et al.•American Journal of Physical…•2013

  • Phenotypic plasticity and constraint along the upper and lower limb diaphyses of H omo sapiens

    Open Access•Jason A Nadell, Colin N Shaw et al.•American Journal of Physical…•2016

  • Ontogenetic changes in magnitudes of integration in the macaque skull

    Open Access•Hyunwoo Jung, Evan A Simons et al.•American Journal of Physical…•2021

  • Evolutionary selection and morphological integration in the vertebral column of modern humans

    Open Access•M Arlegi, Christine Veschambre‐Couture et al.•American Journal of Physical…•2020

  • Bilateral asymmetry of the humerus during growth and development

    Open Access•Amanda Blackburn•American Journal of Physical…•2011

  • Fluctuating and directional asymmetry in the long bones of captive cotton‐top tamarins ( S aguinus oedipus )

    Open Access•Nicole M Reeves, Nicole Reeves et al.•American Journal of Physical…•2016

  • Functional and developmental influences on intraspecific variation in catarrhine vertebrae

    Open Access•Liza J Shapiro, Amanda D Kemp et al.•American Journal of Physical…•2019

  • Morphological integration and natural selection in the postcranium of wild verreaux's sifaka ( Propithecus verreauxi verreauxi )

    Open Access•Richard R Lawler•American Journal of Physical…•2008

  • Intraspecific variability in human maxillary bone modeling patterns during ontogeny

    Open Access•Alexandra Schuh, Philipp Gunz et al.•American Journal of Physical…•2020

  • Limb bone allometry in modern Euro‐Americans

    Open Access•R L Jantz, Lee Meadows Jantz•American Journal of Physical…•2017

  • Bone morphologies and histories

    Open Access•Sabrina C Agarwal•American Journal of Physical…•2016

  • The influence of masticatory loading on craniofacial morphology

    Open Access•Carolina Paschetta, Soledad De Azevedo et al.•American Journal of Physical…•2010

  • A century of development

    Open Access•Joan T Richtsmeier•American Journal of Physical…•2018

  • Hierarchical nature of morphological integration and modularity in the human posterior face

    Open Access•M Bastir, A Rosas•American Journal of Physical…•2005

  • Human life course biology

    Open Access•B Bogin, Carlos Varea et al.•American Journal of Physical…•2018

  • Bilateral asymmetry and developmental plasticity of the humerus in modern humans

    Open Access•Kaya G Zelazny, Adam D Sylvester et al.•American Journal of Physical…•2021

  • Forelimb segment length proportions in extant hominoids and Australopithecus afarensis

    Open Access•M S M Drapeau, Carol V Ward•American Journal of Physical…•2007

  • Morphological integration of anatomical, developmental, and functional postcranial modules in the crab‐eating macaque ( Macaca fascicularis )

    Open Access•Mark A Conaway, Lauren Schroeder et al.•American Journal of Physical…•2018

  • Sifaka positional behavior

    Open Access•Richard R Lawler•American Journal of Physical…•2006

  • Brief communication

    Open Access•Gregory E Blomquist•American Journal of Physical…•2009

  • A resampling approach and implications for estimating the phalangeal index from unassociated hand bones in fossil primates

    Open Access•Vivek V Venkataraman, C Rolian et al.•American Journal of Physical…•2013

  • Covariation between the cranium and the cervical vertebrae in hominids

    Open Access•M Arlegi, Ana Pantoja-Pérez et al.•Journal of Human Evolution•2022

  • Deciphering the correlated evolutionary responses of the hands and feet in modern humans

    Open Access•M Arlegi, Adrián Pablos et al.•Journal of Human Evolution•2025

  • Limb bone bilateral asymmetry

    Open Access•B M Auerbach, C B Ruff•Journal of Human Evolution•2006

  • Trabecular bone structural variation throughout the human lower limb

    Open Access•Jaap Saers, Yasmin Cazorla-Bak et al.•Journal of Human Evolution•2016

  • A reassessment of living hominoid postcranial variability

    Open Access•Nicholas Maurice Young, Nathan M Young•Journal of Human Evolution•2003

  • Multivariate morphometrics, quantitative genetics, and neutral theory

    Open Access•Noreen Von Craman‐taubadel•Evolutionary Anthropology Issues…•2019

  • Bilateral Asymmetry of Long Bones in Bronze and Early Iron Age Pastoralists of the Altai

    Open Access•Tur•Archaeology Ethnology and…•2014

  • Cranial growth in normal and low-protein-fed Saimiri. An environmental heterochrony

    Open Access•Fernando V Ramirez‐rozzi, Fernando V Ramirez Rozzi et al.•Journal of Human Evolution•2005

  • Ontogenetic adaptation to bipedalism

    Open Access•C B Ruff, Christopher Ruff•Journal of Human Evolution•2003

  • Frequency and timing of scaphoid-centrale fusion in hominoids

    Open Access•T L Kivell, David R Begun•Journal of Human Evolution•2007

  • Articular constraint, handedness, and directional asymmetry in the human second metacarpal

    Open Access•Richard A Lazenby, David M L Cooper et al.•Journal of Human Evolution•2008

  • Femoral neck and shaft structure in Homo naledi from the Dinaledi Chamber (Rising Star System, South Africa)

    Open Access•Lukas Friedl, Alex G Claxton et al.•Journal of Human Evolution•2019

  • Morphological integration in the hominid midfoot

    Open Access•Klara Komza, Viola Bence et al.•Journal of Human Evolution•2022

  • Adaptation to suspensory locomotion in Australopithecus sediba

    Open Access•Thomas R Rein, Theo Rein et al.•Journal of Human Evolution•2017

  • Reduced limb integration characterizes primate clades with diverse locomotor adaptations

    Open Access•Jeffrey K Spear•Journal of Human Evolution•2024

  • Morphological evolution through integration

    Open Access•Nandini Singh, K Harvati et al.•Journal of Human Evolution•2012

  • Conserved patterns and locomotor-related evolutionary constraints in the hominoid vertebral column

    Open Access•Catalina I Villamil, Emily R Middleton•Journal of Human Evolution•2024

  • Oblique human symphyseal angle is associated with an evolutionary rate-shift early in the hominin clade

    Open Access•James D Pampush, Jill E Scott et al.•Journal of Human Evolution•2018

  • Human midfacial growth pattern differs from that of Neanderthals and chimpanzees

    Open Access•Alexandra Schuh, Philipp Gunz et al.•Journal of Human Evolution•2025

  • Morphological modularity in the anthropoid axial skeleton

    Open Access•Hyunwoo Jung, Noreen Von Craman‐taubadel et al.•Journal of Human Evolution•2022

  • Locomotor anatomy and biomechanics of the Dmanisi hominins

    Open Access•H Pontzer, C Rolian et al.•Journal of Human Evolution•2010

  • Morphological integration of the hominoid postcranium

    Open Access•Mark A Conaway, Noreen Von Craman‐taubadel•Journal of Human Evolution•2022

  • Developmental Integration and the Evolution of Pleiotropy

    James M Cheverud•American Zoologist•1996

  • A Comparison of Genetic and Phenotypic Correlations

    Open Access•James M Cheverud•Evolution•1988

  • Perspective

    Open Access•Günter P Wagner, Lee Altenberg•Evolution•1996

  • Phenotypic, Genetic, and Environmental Morphological Integration in the Cranium

    Open Access•James M Cheverud•Evolution•1982

  • Canalization of Development and the Inheritance of Acquired Characters

    Open Access•C H Waddington•Nature•1942

  • Fluctuating Asymmetry

    A Richard Palmer, Curtis Strobeck•Annual Review of Ecology and…•1986

  • A Study of Fluctuating Asymmetry

    Open Access•Leigh Van Valen•Evolution•1962

  • Developmental Constraints and Evolution

    John Maynard Smith, Richard M Burian et al.•The Quarterly Review of Biology•1985

  • Fluctuating asymmetry and canalization

    Open Access•B Mohan Reddy•American Journal of Human Biology•1999

  • Genetic and environmental influence on the asymmetry of dermatoglyphic traits

    Open Access•Ekaterina A Pechenkina, R A Benfer et al.•American Journal of Physical…•2000

  • The primate cranial base

    Open Access•D E Lieberman, Callum F Ro et al.•American Journal of Physical…•2000

  • Study of genetic variance in the fluctuating asymmetry of anthropometrical traits

    Open Access•Gregory Livshits, E Kobyliansky•Annals of Human Biology•1989

  • Inbreeding and developmental stability in a small human population

    Open Access•Therese A Markow, John Martin et al.•Annals of Human Biology•1993

  • Fluctuating odontometric asymmetry and maternal alcohol consumption

    Open Access•Julius A Kieser•Annals of Human Biology•1992

  • Dermatoglyphic asymmetry as a measure of canalization

    Open Access•R L Jantz, Robert S Webb•Annals of Human Biology•1980

  • Age-dependent changes in morphometric and biochemical traits

    Open Access•E Kobyliansky, Gregory Livshits•Annals of Human Biology•1989

  • Fluctuating asymmetry inMacaca fascicularis

    Open Access•Benedikt Hallgrimsson•International Journal of…•1993

  • Ontogenetic Patterning of Skeletal Fluctuating Asymmetry in Rhesus Macaques and Humans

    Open Access•Benedikt Hallgrimsson•International Journal of…•1999

  • Developmental correlates of crown component asymmetry and occlusal discrepancy

    Open Access•Robert S Corruccini, Rosario H Potter et al.•American Journal of Physical…•1981

  • Ponderal Index and height

    Open Access•Neil M Huber•American Journal of Physical…•1969

  • Fluctuating dental asymmetry as a measure of odontogenic canalization in man

    Open Access•Julius A Kieser, H T Groeneveld et al.•American Journal of Physical…•1986

  • Fluctuating asymmetry and morphometric variation of hand bones

    Open Access•Gregory Livshits, Konstantin Yakovenko et al.•American Journal of Physical…•1998

  • Ontogeny and phylogeny of femoro-tibial characters in humans and hominid fossils

    Open Access•Christine Tardieu•American Journal of Physical…•1999

  • Fluctuating asymmetry in molar dimensions and discrete morphological traits in Pima Indians

    Open Access•John F Noss, G R Scott et al.•American Journal of Physical…•1983

  • Variability of metapodials in primates with rudimentary digits

    Open Access•R G Tague•American Journal of Physical…•2002

  • Phenotypic covariance structure in tamarins (genusSaguinus)

    Open Access•Rebecca Rogers Ackermann, James M Cheverud•American Journal of Physical…•2000

  • Bilateral asymmetry in skeletal growth and maturation as an indicator of environmental stress

    Open Access•A Midori Albert, D L Greene•American Journal of Physical…•1999

  • Fluctuating asymmetry in fetuses of diabetic rhesus macaques

    Open Access•L A P Kohn, Kenneth A Bennett•American Journal of Physical…•1986

  • On the meaning of increased fluctuating dental asymmetry

    Open Access•William John Doyle, Olivia Johnston•American Journal of Physical…•1977

  • Fluctuating dental asymmetry

    Open Access•Anthony J Perzigian•American Journal of Physical…•1977

  • Genotype, phenotype, and developmental biology of molar tooth characters

    Open Access•Jukka Jernvall, Han‐sung Jung•American Journal of Physical…•2000

  • Primate origins

    Open Access•Mark W Hamrick•Journal of Human Evolution•2001

  • Basicranial influence on overall cranial shape

    Open Access•D E Lieberman, O M Pearson et al.•Journal of Human Evolution•2000

  • Evolution and development of the primate limb skeleton

    Open Access•Chi‐hua Chiu, Chi-Hua Chiu et al.•Evolutionary Anthropology Issues…•2002

  • Dental asymmetry, maternal obesity, and smoking

    Open Access•Jules Kieser, Jules A Kieser et al.•American Journal of Physical…•1997

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Citation span2003 - 2025 (23)
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