Biomechanical evolution of solid bones in large animals: a microanatomical investigation

Graviportal taxa show an allometric increase of the cross-sectional area of supportive bones and are assumed to display microanatomical changes associated with an increase in bone mass. This evokes osteosclerosis (i.e. an increase in bone compactness observed in some aquatic amniotes). The present study investigates the changes in bones' microanatomical organization associated with graviportality and how comparable they are with aquatically acquired osteosclerosis aiming to better understand the adaptation of bone to the different associated functional requirements. Bones of graviportal taxa show microanatomical changes that are not solely attributable to allometry. They display a thicker cortex and a proportionally smaller medullary cavity, with a wider transition zone between these domains. This inner cancellous structure may enable to better enhance energy absorption and marrow support. Moreover, the cross-sectional geometric parameters indicate increased resistance to stresses engendered by bending and torsion, as well as compression. Adaptation to a graviportal posture should be taken into consideration when analyzing possibly amphibious taxa with a terrestrial-like morphology. This is particularly important for palaeoecological inferences about large extinct tetrapods that might have been amphibious and, more generally, for the study of early stages of adaptation to an aquatic life in amniotes.

[1]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[2]  H. Gregory McDonald,et al.  Osteology and Functional Morphology of the Hind Limb of the Marine Sloth Thalassocnus (Mammalia, Tardigrada) , 2015, Journal of Mammalian Evolution.

[3]  Katja Waskow,et al.  Growth Record and Histological Variation in the Dorsal Ribs of Camarasaurus sp. (Sauropoda) , 2014 .

[4]  H. Gregory McDonald,et al.  Osteology and Functional Morphology of the Forelimb of the Marine Sloth Thalassocnus (Mammalia, Tardigrada) , 2014, Journal of Mammalian Evolution.

[5]  J. Hutchinson,et al.  Size-Related Changes in Foot Impact Mechanics in Hoofed Mammals , 2013, PloS one.

[6]  A. Herrel,et al.  Specific information levels in relation to fragmentation patterns of shrew mandibles: do fragments tell the same story? , 2015 .

[7]  C. Ruff,et al.  Long bone articular and diaphyseal structure in old world monkeys and apes. I: locomotor effects. , 2002, American journal of physical anthropology.

[8]  Brian D. Ripley,et al.  Pattern Recognition and Neural Networks , 1996 .

[9]  Scaling of bodily proportions in adult terrestrial mammals. , 1992, The American journal of physiology.

[10]  F. Bibi A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics , 2013, BMC Evolutionary Biology.

[11]  V. Buffrénil,et al.  Evolution of Sirenian Pachyosteosclerosis, a Model-case for the Study of Bone Structure in Aquatic Tetrapods , 2010, Journal of Mammalian Evolution.

[12]  R. McN. Alexander,et al.  The thickness of the walls of tubular bones , 2009 .

[13]  P. D. Polly,et al.  Limbs in Mammalian Evolution , 2006 .

[14]  A. Houssaye,et al.  Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia) , 2015 .

[15]  A. Houssaye,et al.  A New Look at Ichthyosaur Long Bone Microanatomy and Histology: Implications for Their Adaptation to an Aquatic Life , 2014, PloS one.

[16]  R. Alexander,et al.  Locomotion and bone strength of the white rhinoceros, Ceratotherium simum , 1992 .

[17]  M. Carrano,et al.  Implications of limb bone scaling, curvature and eccentricity in mammals and non‐avian dinosaurs , 2001 .

[18]  P Christiansen,et al.  Scaling of the limb long bones to body mass in terrestrial mammals , 1999, Journal of morphology.

[19]  C. Ruff,et al.  Estimating human long bone cross-sectional geometric properties: a comparison of noninvasive methods. , 2004, Journal of human evolution.

[20]  W. P. Wall The correlation between high limb-bone density and aquatic habits in Recent mammals , 1983 .

[21]  P. Tassy,et al.  L’origine et l’évolution des éléphants , 2009 .

[22]  P. Holroyd,et al.  Identifying Aquatic Habits Of Herbivorous Mammals Through Stable Isotope Analysis , 2008 .

[23]  Michel Laurin,et al.  Bone microanatomy and lifestyle: A descriptive approach , 2011 .

[24]  C E Oxnard,et al.  Bone and bones, architecture and stress, fossils and osteoporosis. , 1993, Journal of biomechanics.

[25]  P. Sereno,et al.  The evolution of dinosaurs. , 1999, Science.

[26]  M. Ross The influence of gravity on structure and function of animals. , 1984, Advances in space research : the official journal of the Committee on Space Research.

[27]  J. Skinner,et al.  A comparison of the bone density and morphology of giraffe ( Giraffa camelopardalis ) and buffalo ( Syncerus caffer ) skeletons , 2004 .

[28]  Sandra J. Shefelbine,et al.  Trabecular bone scales allometrically in mammals and birds , 2011, Proceedings of the Royal Society B: Biological Sciences.

[29]  H. Endo,et al.  Turtle humeral microanatomy and its relationship to lifestyle , 2014 .

[30]  C. Gilbert,et al.  Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): Systematics, morphology, and biogeography. , 2006, Molecular phylogenetics and evolution.

[31]  A. Houssaye,et al.  Rib and vertebral micro-anatomical characteristics of hydropelvic mosasauroids , 2012 .

[32]  N. Campione,et al.  A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods , 2012, BMC Biology.

[33]  N. Todd New Phylogenetic Analysis of the Family Elephantidae Based on Cranial‐Dental Morphology , 2010, Anatomical record.

[34]  A. Houssaye,et al.  "Pachyostosis" in aquatic amniotes: a review. , 2009, Integrative zoology.

[35]  V. Buffrénil,et al.  Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates , 2013 .

[36]  A. Garrod Animal Locomotion , 1874, Nature.

[37]  M. Girondot,et al.  BONE PROFILER: A TOOL TO QUANTIFY, MODEL, AND STATISTICALLY COMPARE BONE-SECTION COMPACTNESS PROFILES , 2003 .

[38]  R. Henry,et al.  Anatomy of the Elephant Foot , 2008 .

[39]  L. Marivaux,et al.  Early rhinocerotids (Mammalia: Perissodactyla) from South Asia and a review of the Holarctic Paleogene rhinocerotid record , 2003 .

[40]  Sandra J Shefelbine,et al.  BoneJ: Free and extensible bone image analysis in ImageJ. , 2010, Bone.

[41]  G. Cassini,et al.  On the Evolution of Large Size in Mammalian Herbivores of Cenozoic Faunas of Southern South America , 2012 .

[42]  J. Hokkanen The size of the largest land animal. , 1986, Journal of theoretical biology.

[43]  G. Larson,et al.  The long and winding road: identifying pig domestication through molar size and shape , 2013 .

[44]  T. Garland Phylogenetic comparison and artificial selection , 2001 .

[45]  M. Laurin,et al.  Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences , 2010 .

[46]  P. Barrett,et al.  Phylogeny of the ankylosaurian dinosaurs (Ornithischia: Thyreophora) , 2012 .

[47]  F. Hainsworth Scaling: why is animal size so important? , 1985 .

[48]  E. de Margerie,et al.  Phylogenetic signal in bone microstructure of sauropsids. , 2005, Systematic biology.

[49]  O. Ryder,et al.  Molecular phylogeny and evolution of the Perissodactyla , 2011 .

[50]  Theodore Garland,et al.  Phylogenetic Analysis of Covariance by Computer Simulation , 1993 .

[51]  W. Dabin,et al.  Inner architecture of vertebral centra in terrestrial and aquatic mammals: A two‐dimensional comparative study , 2013, Journal of morphology.

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

[53]  M. Carrano,et al.  Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology , 1998, Paleobiology.

[54]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[55]  T. Osaki,et al.  Bone Inner Structure Suggests Increasing Aquatic Adaptations in Desmostylia (Mammalia, Afrotheria) , 2013, PloS one.

[56]  P. Gingerich,et al.  Transition of Eocene Whales from Land to Sea: Evidence from Bone Microstructure , 2015, PloS one.

[57]  Lei Ren,et al.  Integration of biomechanical compliance, leverage, and power in elephant limbs , 2010, Proceedings of the National Academy of Sciences.

[58]  Kristian Remes Taxonomy of Late Jurassic diplodocid sauropods from Tendaguru (Tanzania) , 2009 .

[59]  V. Buffrénil,et al.  An Analysis of Vertebral ‘Pachyostosis’ In Carentonosaurus Mineaui (Mosasauroidea, Squamata) from the Cenomanian (Early Late Cretaceous) of France, with Comments on its Phylogenetic and Functional Significance , 2008 .

[60]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[61]  Lei Ren,et al.  The movements of limb segments and joints during locomotion in African and Asian elephants , 2008, Journal of Experimental Biology.

[62]  F. Fish,et al.  Functional correlates of differences in bone density among terrestrial and aquatic genera in the family Mustelidae (Mammalia) , 1991, Zoomorphology.

[63]  H. Gunga,et al.  Biology of the sauropod dinosaurs: the evolution of gigantism , 2011, Biological reviews of the Cambridge Philosophical Society.

[64]  A. Herrel,et al.  Amniote vertebral microanatomy – what are the major trends? , 2014 .

[65]  M. Hildebrand Analysis of Vertebrate Structure , 1974 .

[66]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[67]  T. J. Robinson,et al.  Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification , 2011, Science.

[68]  A. Houssaye,et al.  Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia, Squamata) – Implications for Aquatic Adaptation and Growth Rates , 2013, PloS one.

[69]  R. Macphee,et al.  Evolutionary Patterns of Bone Histology and Bone Compactness in Xenarthran Mammal Long Bones , 2013, PloS one.