Microstructural features of the femur in early ophiacodontids: A reappraisal of ancestral habitat use and lifestyle of amniotes

Abstract Ophiacodontids have long been considered the basalmost synapsids, and to have retained a fairly aquatic, piscivorous lifestyle typical of stem-amniotes. A restudy of their bone histology and microanatomy shows that Clepsydrops collettii , a Late Carboniferous ophiacodontid, has a thin, compact cortex and lacks a medullary spongiosa, two features that suggest a truly terrestrial lifestyle. The Early Permian Ophiacodon uniformis has a thicker cortex with a few resorption cavities and bone trabeculae surrounding the free medullary cavity. An inference model yields a terrestrial lifestyle for both taxa, though O. uniformis may have been slightly more aquatic (possibly amphibious) than C. collettii . However, an optimization of inferred lifestyle of other early stegocephalians (based on bone microanatomy) suggests that the first amniotes were terrestrial. The potentially amphibious lifestyle of O. uniformis , though not supported by our inference model, would thus be secondary. Histological features of femoral cortices in these two taxa closely resemble those previously described in extant species of large varanids and teids. This similarity, along with other comparative elements, is discussed in reference to the possible growth patterns and life history traits of Clepsydrops and O. uniformis .

[1]  V. Buffrénil,et al.  Microstructure and Mineralization of Vertebrate Skeletal Tissues , 2013 .

[2]  R. Haines THE EVOLUTION OF EPIPHYSES AND OF ENDOCHONDRAL BONE , 1942 .

[3]  E. de Margerie,et al.  Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos). , 2002, Comptes rendus biologies.

[4]  Denys B. Smith The Permian period , 2019, Geological Society, London, Special Publications.

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

[6]  J. Horner,et al.  On the bone histology of some Triassic pseudosuchian archosaurs and related taxa , 2003 .

[7]  J. Skulan Has the importance of the amniote egg been overstated , 2000 .

[8]  S. Grandin,et al.  Expression de la dynamique de croissance dans la structure de l'os périostique chez Anas platyrhynchos , 1996 .

[9]  M. Laurin,et al.  CRANIAL MORPHOLOGY AND AFFINITIES OF MICROBRACHIS, AND A REAPPRAISAL OF THE PHYLOGENY AND LIFESTYLE OF THE FIRST AMPHIBIANS , 2004 .

[10]  Robert L. Carroll,et al.  Vertebrate Paleontology and Evolution , 1988 .

[11]  M. Laurin,et al.  Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference , 2008, Journal of evolutionary biology.

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

[13]  F. Gradstein,et al.  The Carboniferous Period , 2012 .

[14]  V. Lance Alligator physiology and life history: the importance of temperature , 2003, Experimental Gerontology.

[15]  M. Laurin,et al.  Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda) , 2005 .

[16]  R. Carroll The earliest reptiles , 1964 .

[17]  M. Girondot,et al.  The evolution of long bone microstructure and lifestyle in lissamphibians , 2004, Paleobiology.

[18]  J. Cubo,et al.  Development-based revision of bone tissue classification: the importance of semantics for science , 2014 .

[19]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[20]  D. Enlow,et al.  A comparative histological study of fossil and recent bone tissues. Part III. , 1957 .

[21]  A. Romer,et al.  TETRAPOD LIMBS AND EARLY TETRAPOD LIFE , 1958 .

[22]  K. Martin,et al.  Brave new propagules: terrestrial embryos in anamniotic eggs. , 2013, Integrative and comparative biology.

[23]  K. Angielczyk,et al.  Was Ophiacodon (Synapsida, Eupelycosauria) a Swimmer? A Test Using Vertebral Dimensions , 2014 .

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

[25]  D. Newman,et al.  Skeletochronological data on the growth, age, and population structure of the tuatara, Sphenodon punctatus, on Stephens and Lady Alice islands, New Zealand , 1988 .

[26]  A. Romer,et al.  Review of the Pelycosauria , 1940 .

[27]  M. Laurin Anatomy and relationships of Haptodus garnettensis, a Pennsylvanian synapsid from Kansas , 1993 .

[28]  J. Castanet,et al.  Age Estimation by Skeletochronology in the Nile Monitor (Varanus niloticus), a Highly Exploited Species , 2000 .

[29]  J. G. Carter Skeletal biomineralization : patterns, processes, and evolutionary trends , 1991 .

[30]  M. Benton,et al.  Discussion on ecology of earliest reptiles inferred from basal Pennsylvanian trackwaysJournal, Vol. 164, 2007, 1113–1118 , 2008, Journal of the Geological Society.

[31]  J. Gibbons,et al.  Indeterminate growth in long-lived freshwater turtles as a component of individual fitness , 2012, Evolutionary Ecology.

[32]  M. Buchwitz,et al.  On the use of osteoderm features in a phylogenetic approach on the internal relationships of the Chroniosuchia (Tetrapoda: Reptiliomorpha) , 2012 .

[33]  A. Huttenlocker,et al.  Comparative anatomy and osteohistology of hyperelongate neural spines in the sphenacodontids Sphenacodon and Dimetrodon (Amniota: Synapsida) , 2010, Journal of morphology.

[34]  S. Lucas Global Permian tetrapod biostratigraphy and biochronology , 2006, Geological Society, London, Special Publications.

[35]  V. Buffrénil,et al.  Geometric and metabolic constraints on bone vascular supply in diapsids , 2014 .

[36]  P. Ahlberg,et al.  Tetrapod trackways from the early Middle Devonian period of Poland , 2010, Nature.

[37]  R. Ryan,et al.  Stratigraphy and sedimentology of early Pennsylvanian red beds at Lower Cove, Nova Scotia, Canada: the Little River Formation with redefinition of the Joggins Formation , 2006 .

[38]  A. Houssaye,et al.  Bone vascular supply in monitor lizards (Squamata: Varanidae): Influence of size, growth, and phylogeny , 2008, Journal of morphology.

[39]  O. B. Goin,et al.  AMPHIBIAN EGGS AND THE MONTANE ENVIRONMENT , 1962 .

[40]  R. Reisz,et al.  The cranial anatomy and relationships of Secodontosaurus, an unusual mammal-like reptile (Synapsida: Sphenacodontidae) from the early Permian of Texas , 1992 .

[41]  E. Margerie,et al.  Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus) , 2004, Journal of Experimental Biology.

[42]  H. Messel,et al.  Growth Rates of Crocodylus Porosus (Reptilia: Crocodilia) From Arnhem Land, Northern Australia. , 1978 .

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

[44]  J. Horner,et al.  Osteohistological Evidence for Determinate Growth in the American Alligator , 2011 .

[45]  K. Adam,et al.  Analysis of Growth Rates , 2013 .

[46]  M. Báez,et al.  Adaptation and evolution in Gallotia lizards from the Canary Islands: age, growth, maturity and longevity , 1991 .

[47]  A. Romer The primitive reptile Limnoscelis restudied , 1946 .

[48]  L. Brand,et al.  Fossil vertebrate footprints in the Coconino Sandstone (Permian) of northern Arizona: Evidence for underwater origin , 1991 .

[49]  Vivian de Buffrénil,et al.  Variation in Longevity, Growth, and Morphology in Exploited Nile Monitors (Varanus niloticus) from Sahelian Africa , 2002 .

[50]  R. Benson Interrelationships of basal synapsids: cranial and postcranial morphological partitions suggest different topologies , 2012 .