Clarifying Tetrapod Embryogenesis, a Physicist's Point of View

Eur. Phys. J. Appl. Phys. 45, 30101 (2009) DOI: 10.1051/epjap/2009033 THE EUROPEAN PHYSICAL JOURNAL APPLIED PHYSICS Clarifying tetrapod embryogenesis, a physicist’s point of view V. Fleurya CNRS/Institut de Physique de Rennes, Université de Rennes 1, 35042 Rennes, France Received: 10 June 2008 / Accepted: 26 January 2009 Published online: 11 March 2009 – c EDP Sciences Abstract. The origin of tetrapods is a complex question that webs together genetic, paleontological, developmental and physical facts. Basically, the development of embryos is described by a complex mix of mechanical movements and biochemical inductions of genetic origin. It is difficult to sort out in this sci- entific question what are the fundamental features imposed by conservation laws of physics, and by force equilibria, and what can be ascribed to successive, very specific, stop-and-go inductions of genetic nature. A posteriori, evolution selects the parameters of this process as found in the observed species. Whether there is a general law to animal formation seems out of the question. However, several concepts developed in biology, like the concept of “organizer” seem questionable from a physics point of view, since the entire deformation and force field should be the “organizer” of development, and one can hardly ascribe such a role to a single small area of the embryo body. In the same spirit, the concept of “positional information” encapsulated in concentration of chemicals seems questionable since the deformation and force fields in embryonic tissues are tensors. Finally, the concept of a development organized in space along three orthogonal (“Cartesian”) axes associated to chemical gradients seems also questionable, since early embryo development is driven by complex vortex fields, with hyperbolic trajectories which span the entire embryo. Such hyperbolic trajectories are best understood by a description in terms of dipolar components of the morphogenetic forces, whose projections along orthogonal axes have no specific meaning except as a math- ematical tool. I review here the present state of description of several aspects of tetrapods morphogenesis and evolution, from the point of view of physics. It is getting clear that several basic features of tetrapods body are a direct consequences of fundamental laws of physics. Several lines of work reviewed here show that the topology of the tetrapods may be directly related to the structure of the earliest movements in embryos. The bio-mechanical approach leads to important consequences for the constraints on evolution of the craniates. Such consequences have received a controversial welcome in the last decade, although they may encapsulate the true origin of craniates, esp. simians, and eventually homo. PACS. 87.19.lx Development and growth – 87.18.-h Biological complexity – 68.15.+e Liquid thin films 1 Introduction One may expect the field ui (x, y, z, t) to contain all the physical parameters of genetic origin. Understanding the There is no need to explain that animal embryos, espe- development of an animal requires then to find the dis- cially vertebrates, are material “things”. As such they placement rate field, as a function of all chemicals in the develop following the laws of condensed matter physics, problem, which may seem a formidable task. In order to do especially Newton’s law for deformations (elasticity laws) so, a classical approach in physics consists in finding the and deformation rates (viscous materials). A complete de- relationship between deformation rates, stresses and vol- scription of animal body formation should end by finding ume forces, and encapsulate this relationship into a con- stitutive equation for the said material. the entire morphogenetic field. An animal Ai should be written in terms of its fertilized ovocyte Oi and the dis- The genetic approach is completely different. It is as- placement rate vector ui: sumed that genes, being the true parameters of the developmental process, determine completely animal traits, and T that finding the entire set of genes playing a role in the Ai(x, y, z, T )=Oi (x, y, z)+ ui(x, y, z, t)dt. 0 problem, and the way they influence each other, should clarify the problem of animal development. Since genes a Present address: Laboratoire Matière et Systèmes Com- may be altered or duplicated during cell division mishaps plexes, Université de Paris VII-Denis Diderot, 75013 Paris, (leading eventually to new species), and since modifica- France. tion of genes may modify the complex set of inductive ac- e-mail: [email protected] tions, a precise description of body formation may require Article published by EDP Sciences The European Physical Journal Applied Physics a fantastic analysis of lots of genetically chained reactions. In this spirit, there would exist a few master genes which organize body axis, like bicoid or nanos, and homeotic Hox genes [1], which influence other genes which are found “downstream”, and determine the exact shape of localized body parts by chemical modification of proteins (either concentrations, timing or interactions). Also, due to hi- erarchical construction of the genetic reaction networks, there would exist specific robust genetic regulatory ker- nels, which are less likely to evolve during evolution [2,3]. Understanding gross morphological traits would con- sist in understanding the interplay of the main master genes, before going into more detailed features (e.g.: hav- ing feathers or hairs, hooves or nails, etc.). A considerable activity exists in this field of developmental biology, especially in relation to the fly model drosophila, but it is getting increasingly evident that fly morphogenesis is quite different from vertebrate morphogenesis. In terms of animal description, paleontology lies in between physics and genetics. Indeed, in many cases pale- ontologists are able to describe the transition from one form to another, by analyzing in detail shifts, or drifts, in body parts, e.g. neck or tail elongation [4], or transition from plantigrades (animals walking on the sole, like hu- mans) to digitigrades (animals walking on the fingers, like dogs) [5](Fig.1), but it is very rare that direct genetic data may have been preserved in fossils, except the latest ones [6]. Therefore, genetic analysis of developmental shifts of traits between extinct species is difficult. Shifts of traits as Fig. 1. Transition from digitigrades to unguligrades1.The observed on species are ascribed to selection of improved plate represents the bone structure of animals as found in the traits, in terms of adaptation, but traits should be able fossil record, with transitional forms from plantigrades to dig- to shift, in the first place. In this rationale, traits appear itigrades and unguligrades (From Ref. [5]). The fossil records first in a small group of animals, possibly one single in- shows animal species with progressive limb extension, these ex- dividual, and then spread by Darwinian selection of the tensions correlate with reduction of lateral fingers. The lateral fittest, with possible subtleties like accelerated selection fingers may remain as vestigial, almost useless phalanges. in geographically isolated groups of individuals (punctu- ated equilibrium, etc.) [7]. There exist bitter controversies about the dynamics of natural selection [8,9]. However, the other by formal spatio-temporal mechanical fields in the paleontological description of how traits actually appear, space of shapes. before being selected, is interesting from the point of view Therefore, there is a possibility that animal formation of physics: anatomical traits seem to “derive” or “drift” may be understood on the basis of physical principles in from previous traits. Folds seem to “extend”, joints “ro- the following way: genetic parameters, and their inductive tate”, body parts “expand”, vestigial organs progressively relationships set a number of mechanical properties, such “reduce”. This wording assumes implicitly some mechani- as material constants, instability parameters and volume cal feature, and the existence of dimensionless traits which forces, then the integral during development in each in- can be scaled up or down, wound and rewound, elongated dividual of the deformation rate tensor gives the animal or stretched arbitrarily, in a space of latent forms. shape at birth. A modified individual shape corresponds to a different set of input genetic parameters, and selec- It has long been recognized, for example in the clas- tion acts a posteriori on the modified shape to stabilize sical observations of D’Arcy Thomson [10](Fig.2), that the species and maintain it over a significantly long time, animal forms may often be obtained one from each other such that the species may be present in the fossil record by seemingly simple distortion maps, i.e., by a simple inte- at all. Consider two animals belonging to different species, gral over an abstract space-time “on paper” of a physical deformation rate field. This is to say that, although two 1 It is interesting to note that there exists even in human animal species are formed of different individuals, which a condition called “equine walk”, by which children, and even developed in different eggs or wombs at different times, adults have a digitigrade walk. In some instances this condition it seems that one can construct an abstract geometrical is related to tendon shortening. In other cases, no particular space in which species forms can be deformed into one an- pathology is found, and these patients just walk like that. 30101-p2 V. Fleury: Clarifying tetrapod embryogenesis Fig. 2. Anamorphosis maps proposed by d’Arcy Thomson. From On growth and form [10]. D’Arcy Thomson had the intuition that different animal forms could be related by simple macroscopic deformations acting on the same qualitative pattern (stated otherwise, a “dimensionless” archetypic animal can be mapped onto other species by affine transformations). if they are formed by the same developmental process, al- lected among an infinite set of possible, but not selected, though with different biomechanical parameters, they will shapes.

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