Morphological Integration in Mammalian Limb Proportions: Dissociation between Function and Development

During mammalian evolution, fore- and hindlimbs underwent a fundamental reorganization in the transformation from the sprawled to the parasagittal condition. This caused a dissociation between serial and functional homologues. The mobilized scapula functions as the new proximal forelimb element and is functionally analogous to the femur of the hindlimb. Tarsus and metatarsus built a new functional hindlimb element that is functionally analogous to the forearm of the forelimb. Morphological covariation between serially homologous fore- and hindlimb elements can conflict with biomechanical demands when certain intralimb proportions are required for the postural stability of motion. The limb proportions of 189 mammalian species were examined to test whether intralimb proportions are governed by a general principle that corresponds to biomechanical predictions. Morphological covariation between functionally analogous and serially homologous fore- and hindlimb elements was tested by a correlation analysis. A clear relationship exists between the proportions of the first and the third elements of each limb, while the middle element is less involved in alterations of intralimb proportions. Hindlimb proportions are largely uniform across mammals and correspond to biomechanical predictions regarding postural stability. The greater variability in forelimb proportion is likely be the expression of various adaptations but might results also from constraints due to the shared developmental programs with the hindlimb.

[1]  A. Bennett The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[2]  William K. Gregory,et al.  NOTES ON THE PRINCIPLES OF QUADRUPEDAL LOCOMOTION AND ON THE MECHANISM OF HE LIMBS IN HOOFED ANIMALS , 1912 .

[3]  William L. Engels Cursorial adaptations in birds. Limb proportions in the skeleton of geococcyx , 1938 .

[4]  Richard C. Snyder,et al.  Quadrupedal and Bipedal Locomotion of Lizards , 1952 .

[5]  M. Hildebrand An analysis of body proportions in the Canidae. , 1952, The American journal of anatomy.

[6]  A. Lundberg,et al.  Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles , 1958, The Journal of physiology.

[7]  M. Hildebrand Body proportions of didelphid (and some other) marsupials, with emphasis on variability. , 1961, The American journal of anatomy.

[8]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[9]  Yosef Hochberg,et al.  Some generalizations of the T-method in simultaneous inference , 1974 .

[10]  T. McMahon Using body size to understand the structural design of animals: quadrupedal locomotion. , 1975, Journal of applied physiology.

[11]  W. Gonyea Adaptive differences in the body proportions of large felids. , 1976, Acta Anatomica.

[12]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  W. Jungers Locomotion, limb proportions, and skeletal allometry in lemurs and lorises. , 1979, Folia primatologica; international journal of primatology.

[14]  J. Fleagle,et al.  Postnatal growth allometry of the extremities in Cebus albifrons and Cebus apella: a longitudinal and comparative study. , 1980, American journal of physical anthropology.

[15]  G. E. Goslow,et al.  The functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus) , 1983, Journal of morphology.

[16]  C. G. Phillips,et al.  The pattern of monosynaptic I a-connections to hindlimb motor nuclei in the baboon: a comparison with the cat , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  C. Pond,et al.  Walker's Mammals of the World, 4th Edition, Ronald M. Nowak, John L. Paradiso. The Johns Hopkins University Press, Baltimore, Maryland (1983), 1xi, +1-568 (Vol. I), xxv+569-1362 (Vol. II). Price $65.00 , 1984 .

[18]  V. Roth How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species , 1984 .

[19]  William L. Jungers,et al.  Body Size and Scaling of Limb Proportions in Primates , 1985 .

[20]  R. Wayne,et al.  Limb morphology of domestic and wild canids: The influence of development on morphologic change , 1986, Journal of morphology.

[21]  Gerrit Jan VAN INGEN SCHENAU,et al.  From rotation to translation: Constraints on multi-joint movements and the unique action of bi-articular muscles , 1989 .

[22]  S. Gatesy,et al.  Bipedal locomotion: effects of speed, size and limb posture in birds and humans , 1991 .

[23]  S. Gatesy Hind limb scaling in birds and other theropods: Implications for terrestrial locomotion , 1991, Journal of morphology.

[24]  C. Tabin,et al.  Hox genes and serial homology , 1993, Nature.

[25]  Denis Duboule,et al.  Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs , 1993, Cell.

[26]  Theodore Garland,et al.  Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? , 1993 .

[27]  K. Steudel,et al.  Scaling of cursoriality in mammals , 1993, Journal of morphology.

[28]  J. P. Wells,et al.  Ontogeny of locomotion in rhesus macaques (Macaca mulatta): I. Early postnatal ontogeny of the musculoskeletal system , 1994 .

[29]  M. Fischer Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea) , 1994 .

[30]  B. Hall Homology and Embryonic Development , 1995 .

[31]  N. Rowe The Pictorial Guide to the Living Primates , 1996 .

[32]  V. Papaioannou,et al.  Evidence of a role for T-☐ genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity , 1996, Mechanisms of Development.

[33]  Gerd B. Müller,et al.  Homology, Hox Genes, and Developmental Integration , 1996 .

[34]  S. Carroll,et al.  Fossils, genes and the evolution of animal limbs , 1997, Nature.

[35]  C. Tabin,et al.  Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. , 1997, Development.

[36]  C. Tabin,et al.  Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity. , 1998, Development.

[37]  C. Tabin,et al.  Role of Pitx1 upstream of Tbx4 in specification of hindlimb identity. , 1999, Science.

[38]  M. Illert,et al.  Monosynaptic Ia pathways at the cat shoulder , 1999, The Journal of physiology.

[39]  K. Patel,et al.  Dual origin and segmental organisation of the avian scapula. , 2000, Development.

[40]  I. Ruvinsky,et al.  Genetic and developmental bases of serial homology in vertebrate limb evolution. , 2000, Development.

[41]  Reinhard Blickhan,et al.  Stable operation of an elastic three-segment leg , 2001, Biological Cybernetics.

[42]  Serafino Pantano,et al.  Agenesis of the scapula in Emx2 homozygous mutants. , 2001, Developmental biology.

[43]  J. Gasc,et al.  Comparative aspects of gait, scaling and mechanics in mammals. , 2000, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[44]  Martin S. Fischer,et al.  Locomotory organs of Mammals: New mechanics and feed-back pathways but conservative central control , 2001 .

[45]  Benedikt Hallgrímsson,et al.  Canalization, developmental stability, and morphological integration in primate limbs. , 2002, American journal of physical anthropology.

[46]  R. German,et al.  Ontogenetic allometry in the locomotor skeleton of specialized half-bounding mammals , 2002 .

[47]  M. Fischer,et al.  Basic limb kinematics of small therian mammals. , 2002, The Journal of experimental biology.

[48]  L. Johansson,et al.  Functional correlation between habitat use and leg morphology in birds (Aves) , 2003 .

[49]  M. Capecchi,et al.  Materials and Methods Som Text Figs. S1 to S4 Tables S1 and S2 References and Notes Hox10 and Hox11 Genes Are Required to Globally Pattern the Mammalian Skeleton , 2022 .

[50]  Martin S. Fischer,et al.  Scaling of long bones in ruminants with respect to the scapula , 2003 .

[51]  Nathan M. Young Modularity and integration in the hominoid scapula. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[52]  M. Capecchi,et al.  Multiple roles of Hoxa11 and Hoxd11 in the formation of the mammalian forelimb zeugopod , 2003, Development.

[53]  M. Ashley-Ross,et al.  Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa , 2004, Journal of Experimental Biology.

[54]  B. Hallgrímsson,et al.  SERIAL HOMOLOGY AND THE EVOLUTION OF MAMMALIAN LIMB COVARIATION STRUCTURE , 2005, Evolution; international journal of organic evolution.

[55]  R. Blickhan,et al.  The tri-segmented limbs of therian mammals: kinematics, dynamics, and self-stabilization--a review. , 2006, Journal of experimental zoology. Part A, Comparative experimental biology.

[56]  N. Schilling,et al.  Postnatal allometry of the skeleton in Tupaia glis (Scandentia: Tupaiidae) and Galea musteloides (Rodentia: Caviidae)--a test of the three-segment limb hypothesis. , 2006, Zoology.

[57]  Michael Günther,et al.  Intelligence by mechanics , 2007, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[58]  L. M. Day,et al.  Interspecific scaling of the morphology and posture of the limbs during the locomotion of cats (Felidae) , 2007, Journal of Experimental Biology.

[59]  Denis Duboule,et al.  The role of Hox genes during vertebrate limb development. , 2007, Current opinion in genetics & development.

[60]  Manuela Schmidt,et al.  Forelimb proportions and kinematics: how are small primates different from other small mammals? , 2005, Journal of Experimental Biology.

[61]  R. McN. Alexander,et al.  Fast locomotion of some African ungulates , 2009 .