Julia Molnar

A new heart for a new head in vertebrate cardiopharyngeal evolution

It has been more than 30 years since the publication of the new head hypothesis, which proposed that the vertebrate head is an evolutionary novelty resulting from the emergence of neural crest and cranial placodes. Neural crest generates the skull and associated connective tissues, whereas placodes produce sensory organs. However, neither crest nor placodes produce head muscles, which are a crucial component of the complex vertebrate head. We discuss emerging evidence for a surprising link between the evolution of head muscles and chambered hearts — both systems arise from a common pool of mesoderm progenitor cells within the cardiopharyngeal field of vertebrate embryos. We consider the origin of this field in non-vertebrate chordates and its evolution in vertebrates.

A Computational Analysis of Limb and Body Dimensions in Tyrannosaurus rex with Implications for Locomotion, Ontogeny, and Growth

The large theropod dinosaur Tyrannosaurus rex underwent remarkable changes during its growth from <10 kg hatchlings to >6000 kg adults in <20 years. These changes raise fascinating questions about the morphological transformations involved, peak growth rates, and scaling of limb muscle sizes as well as the bodys centre of mass that could have influenced ontogenetic changes of locomotion in T. rex. Here we address these questions using three-dimensionally scanned computer models of four large, well-preserved fossil specimens as well as a putative juvenile individual. Furthermore we quantify the variations of estimated body mass, centre of mass and segment dimensions, to characterize inaccuracies in our reconstructions. These inaccuracies include not only subjectivity but also incomplete preservation and inconsistent articulations of museum skeletons. Although those problems cause ambiguity, we conclude that adult T. rex had body masses around 6000–8000 kg, with the largest known specimen (“Sue”) perhaps ∼9500 kg. Our results show that during T. rex ontogeny, the torso became longer and heavier whereas the limbs became proportionately shorter and lighter. Our estimates of peak growth rates are about twice as rapid as previous ones but generally support previous methods, despite biases caused by the usage of scale models and equations that underestimate body masses. We tentatively infer that the hindlimb extensor muscles masses, including the large tail muscle M. caudofemoralis longus, may have decreased in their relative size as the centre of mass shifted craniodorsally during T. rex ontogeny. Such ontogenetic changes would have worsened any relative or absolute decline of maximal locomotor performance. Regardless, T. rex probably had hip and thigh muscles relatively larger than any extant animals. Overall, the limb “antigravity” muscles may have been as large as or even larger than those of ratite birds, which themselves have the most muscular limbs of any living animal.

Vertebral architecture in the earliest stem tetrapods

The construction of the vertebral column has been used as a key anatomical character in defining and diagnosing early tetrapod groups. Rhachitomous vertebrae—in which there is a dorsally placed neural arch and spine, an anteroventrally placed intercentrum and paired, posterodorsally placed pleurocentra—have long been considered the ancestral morphology for tetrapods. Nonetheless, very little is known about vertebral anatomy in the earliest stem tetrapods, because most specimens remain trapped in surrounding matrix, obscuring important anatomical features. Here we describe the three-dimensional vertebral architecture of the Late Devonian stem tetrapod Ichthyostega using propagation phase-contrast X-ray synchrotron microtomography. Our scans reveal a diverse array of new morphological, and associated developmental and functional, characteristics, including a possible posterior-to-anterior vertebral ossification sequence and the first evolutionary appearance of ossified sternal elements. One of the most intriguing features relates to the positional relationships between the vertebral elements, with the pleurocentra being unexpectedly sutured or fused to the intercentra that directly succeed them, indicating a ‘reverse’ rhachitomous design. Comparison of Ichthyostega with two other stem tetrapods, Acanthostega and Pederpes, shows that reverse rhachitomous vertebrae may be the ancestral condition for limbed vertebrates. This study fundamentally revises our current understanding of vertebral column evolution in the earliest tetrapods and raises questions about the presumed vertebral architecture of tetrapodomorph fish and later, more crownward, tetrapods.

Comparative Anatomy, Evolution, and Homologies of Tetrapod Hindlimb Muscles, Comparison with Forelimb Muscles, and Deconstruction of the Forelimb‐Hindlimb Serial Homology Hypothesis

For more than two centuries, the idea that the forelimb and hindlimb are serially homologous structures has been accepted without serious question. This study presents the first detailed analysis of the evolution and homologies of all hindlimb muscles in representatives of each major tetrapod group and proposes a unifying nomenclature for these muscles. These data are compared with information obtained previously about the forelimb muscles of tetrapods and the muscles of other gnathostomes in order to address one of the most central and enigmatic questions in evolutionary and comparative anatomy: why are the pelvic and pectoral appendages of gnathostomes generally so similar to each other? An integrative analysis of the new myological data, combined with a review of recent paleontological, developmental, and genetic works and of older studies, does not support serial homology between the structures of these appendages. For instance, many of the strikingly similar forelimb and hindlimb muscles found in each major extant tetrapod taxon were acquired at different geological times and/or have different embryonic origins. These similar muscles are not serial homologues, but the result of evolutionary parallelism/convergence due to a complex interplay of ontogenetic, functional, topological, and phylogenetic constraints/factors. Anat Rec, 297:1047–1075, 2014.

An experimental and morphometric test of the relationship between vertebral morphology and joint stiffness in Nile crocodiles (Crocodylus niloticus)

Despite their semi-aquatic mode of life, modern crocodylians use a wide range of terrestrial locomotor behaviours, including asymmetrical gaits otherwise only found in mammals. The key to these diverse abilities may lie in the axial skeleton. Correlations between vertebral morphology and both intervertebral joint stiffness and locomotor behaviour have been found in other animals, but the vertebral mechanics of crocodylians have not yet been experimentally and quantitatively tested. We measured the passive mechanics and morphology of the thoracolumbar vertebral column in Crocodylus niloticus in order to validate a method to infer intervertebral joint stiffness based on morphology. Passive stiffness of eight thoracic and lumbar joints was tested in dorsal extension, ventral flexion and mediolateral flexion using cadaveric specimens. Fifteen measurements that we deemed to be potential correlates of stiffness were taken from each vertebra and statistically tested for correlation with joint stiffness. We found that the vertebral column of C. niloticus is stiffer in dorsoventral flexion than in lateral flexion and, in contrast to that of many mammals, shows an increase in joint stiffness in the lumbar region. Our findings suggest that the role of the axial column in crocodylian locomotion may be functionally different from that in mammals, even during analogous gaits. A moderate proportion of variation in joint stiffness (R2=0.279–0.520) was predicted by centrum width and height, neural spine angle and lamina width. These results support the possible utility of some vertebral morphometrics in predicting mechanical properties of the vertebral column in crocodiles, which also should be useful for forming functional hypotheses of axial motion during locomotion in extinct archosaurs.

Comparative architectural properties of limb muscles in Crocodylidae and Alligatoridae and their relevance to divergent use of asymmetrical gaits in extant Crocodylia

Crocodiles and their kin (Crocodylidae) use asymmetrical (bounding and galloping) gaits when moving rapidly. Despite being morphologically and ecologically similar, it seems alligators and their kin (Alligatoridae) do not. To investigate a possible anatomical basis for this apparent major difference in locomotor capabilities, we measured relative masses and internal architecture (fascicle lengths and physiological cross‐sectional areas) of muscles of the pectoral and pelvic limbs of 40 individuals from six representative species of Crocodylidae and Alligatoridae. We found that, relative to body mass, Crocodylidae have significantly longer muscle fascicles (increased working range), particularly in the pectoral limb, and generally smaller muscle physiological cross‐sectional areas (decreased force‐exerting capability) than Alligatoridae. We therefore hypothesise that the ability of some crocodylians to use asymmetrical gaits may be limited more by the ability to make large, rapid limb motions (especially in the pectoral limb) than the ability to exert large limb forces. Furthermore, analysis of scaling patterns in muscle properties shows that limb anatomy in the two clades becomes more divergent during ontogeny. Limb muscle masses, fascicle lengths and physiological cross‐sectional areas scale with significantly larger coefficients in Crocodylidae than Alligatoridae. This combination of factors suggests that inter‐clade disparity in maximal limb power is highest in adult animals. Therefore, despite their apparent morphological similarities, both mean values and scaling patterns suggest that considerable diversity exists in the locomotor apparatus of extant Crocodylia.

Morphological and functional changes in the vertebral column with increasing aquatic adaptation in crocodylomorphs

The lineage leading to modern Crocodylia has undergone dramatic evolutionary changes in morphology, ecology and locomotion over the past 200+ Myr. These functional innovations may be explained in part by morphological changes in the axial skeleton, which is an integral part of the vertebrate locomotor system. Our objective was to estimate changes in osteological range of motion (RoM) and intervertebral joint stiffness of thoracic and lumbar vertebrae with increasing aquatic adaptation in crocodylomorphs. Using three-dimensional virtual models and morphometrics, we compared the modern crocodile Crocodylus to five extinct crocodylomorphs: Terrestrisuchus, Protosuchus, Pelagosaurus, Steneosaurus and Metriorhynchus, which span the spectrum from terrestrial to fully aquatic. In Crocodylus, we also experimentally measured changes in trunk flexibility with sequential removal of osteoderms and soft tissues. Our results for the more aquatic species matched our predictions fairly well, but those for the more terrestrial early crocodylomorphs did not. A likely explanation for this lack of correspondence is the influence of other axial structures, particularly the rigid series of dorsal osteoderms in early crocodylomorphs. The most important structures for determining RoM and stiffness of the trunk in Crocodylus were different in dorsoventral versus mediolateral bending, suggesting that changes in osteoderm and rib morphology over crocodylomorph evolution would have affected movements in some directions more than others.

Bonobo anatomy reveals stasis and mosaicism in chimpanzee evolution, and supports bonobos as the most appropriate extant model for the common ancestor of chimpanzees and humans

Common chimps and bonobos are our closest living relatives but almost nothing is known about bonobo internal anatomy. We present the first phylogenetic analysis to include musculoskeletal data obtained from a recent dissection of bonobos. Notably, chimpanzees, and in particular bonobos, provide a remarkable case of evolutionary stasis for since the chimpanzee-human split c.8 Ma among >120 head-neck (HN) and forelimb (FL) muscles there were only four minor changes in the chimpanzee clade, and all were reversions to the ancestral condition. Moreover, since the common chimpanzee-bonobo split c.2 Ma there have been no changes in bonobos, so with respect to HN-FL musculature bonobos are the better model for the last common ancestor (LCA) of chimpanzees/bonobos and humans. Moreover, in the hindlimb there are only two muscle absence/presence differences between common chimpanzees and bonobos. Puzzlingly, there is an evolutionary mosaicism between each of these species and humans. We discuss these data in the context of available genomic information and debates on whether the common chimpanzee-bonobo divergence is linked to heterochrony.

Characteristic tetrapod musculoskeletal limb phenotype emerged more than 400 MYA in basal lobe-finned fishes

Previous accounts of the origin of tetrapod limbs have postulated a relatively sudden change, after the split between extant lobe-finned fish and tetrapods, from a very simple fin phenotype with only two muscles to the highly complex tetrapod condition. The evolutionary changes that led to the muscular anatomy of tetrapod limbs have therefore remained relatively unexplored. We performed dissections, histological sections, and MRI scans of the closest living relatives of tetrapods: coelacanths and lungfish. Combined with previous comparative, developmental and paleontological information, our findings suggest that the characteristic tetrapod musculoskeletal limb phenotype was already present in the Silurian last common ancestor of extant sarcopterygians, with the exception of the autopod (hand/foot) structures, which have no clear correspondence with fish structures. Remarkably, the two major steps in this long process – leading to the ancestral fin anatomy of extant sarcopterygians and limb anatomy of extant tetrapods, respectively – occurred at the same nodes as the two major similarity bottlenecks that led to the striking derived myological similarity between the pectoral and pelvic appendages within each taxon. Our identification of probable homologies between appendicular muscles of sarcopterygian fish and tetrapods will allow more detailed reconstructions of muscle anatomy in early tetrapods and their relatives.

Idealized landmark-based geometric reconstructions of poorly preserved fossil material: a case study of an early tetrapod vertebra

Three-dimensional (3D) digital models of bone morphology are used frequently in paleontology and anthropology. Because fossils are often fragmentary or distorted, it often becomes necessary, for either aesthetic or practical reasons, to create an idealized version of digital skeletons. We propose a method for building landmark-based geometric reconstructions of fossil bones in 3D graphics software using CT or laser scan data as a template. This method does not require specialized software or artistic expertise. It allows control of local mesh density, specification of important landmarks and major planes, elimination of large holes and extraneous structures, and interactive adjustment of 3D shape by moving a small number of vertices to correct minor taphonomic deformation. The result is a simple, illustrative, and accurate model that can be used for diverse analytical and visualization applications, including reconstructions of incomplete fossils, watertight models for mass and center of mass approximation, base meshes for thin plate spline warping, and intermediates in an incomplete series via “morphing.” To demonstrate the method, we applied it to reconstruct a dorsal vertebra from the basal tetrapod Acanthostega gunnari. We validated our methodology with linear and geometric morphometric comparisons of our reconstructions both against the original scan data and between three different operators. Based upon four linear measurements, the average deviation of the models from the original was minimal, showing that the method preserves the proportions of the original fossil. We found no statistically significant shape difference between models built by different operators, demonstrating that the method is repeatable. Julia L. Molnar. Department of Veterinary Basic Sciences and Structure and Motion Laboratory, The Royal Veterinary College, AL97TA, United Kingdom. jmolnar@rvc.ac.uk Stephanie E. Pierce. University Museum of Zoology, Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, United Kingdom and Department of Veterinary Basic Sciences and Structure and Motion Laboratory, The Royal Veterinary College, AL97TA, United Kingdom spierce@rvc.ac.uk Jennifer A. Clack. Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, United Kingdom j.a.clack@zoo.cam.ac.uk PE Article Number: 15.1.2T Copyright: Palaeontological Association February 2012 Submission: 16 March 2011. Acceptance: 22 November 2011 Molnar, Julia L., Pierce, Stephanie E., Clack, Jennifer A., and Hutchinson, John R.. 2012. Idealized landmark-based geometric reconstructions of poorly preserved fossil material: a case study of an early tetrapod vertebra. Palaeontologia Electronica Vol. 15,