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Embryo geometry: a theory of evolution from a single cell to the complex vertebrate body

Embryo geometry: a theory of evolution from a single cell to the complex vertebrate body

One of biology’s biggest mysteries is the genesis of animal form. Biologists trying to understand the genesis and evolution of life have studied and sought to characterize the embryology of all multicellular animal phyla since the 19th century. Many people believed that by the turn of the twentieth century, this work would have been completed.

Anatomists have succeeded in giving comprehensive descriptions of the musculoskeletal, organ, and neurological systems, ranging from Leonardo Da Vinci and Vesalius through Gray’s Anatomy. However, the genesis of these and other elements of organismal shape remains a mystery. Because the body develops from the embryo, nineteenth-century anatomists logically sought a solution by observing early animal development—or embryogenesis. By the end of the nineteenth century, virtually all major phyla’s embryological phases had been described in minute detail.

Major evolutionary changes, according to Neo-Darwinian theory, occur as a result of the selection of random, fortunate genetic mutations through time. However, other experts argue that this hypothesis fails to account for the emergence of fundamentally diverse living forms and their rich complexity, notably in vertebrates like humans.

The authors beg the reader to suspend skepticism that such a complex and longstanding problem is subject to a solution of relative simplicity. “Embryo geometry”, developed by a team from the University of San Diego, Mount Holyoke College, Evergreen State College, and Chem-Tainer Industries, Inc. in the United States, considers animal complexity in general, and the vertebrate body in particular, to be the result of mechanical forces and geometric laws rather than random genetic mutation.

They offer 24 “blueprints” in their article that illustrate how the musculoskeletal, cardiovascular, neurological, and reproductive systems evolve through the mechanical deformation of geometric patterns. These images show how the vertebrate body might have evolved from a single cell during the evolutionary time and during individual development.

Though neither rigorous nor exhaustive in an empirical sense, our model offers an intuitive and plausible description of the emergence of form via simple geometrical and mechanical forces and constraints. The model provides a template, or roadmap, for further investigation, subject to confirmation (or refutation) by interested researchers.

Fig. 1. Blastulation, gastrulation, and embryonic fate map. a. Egg; b–f. Cleavage; g-h. Gastrulation; i. Schematic ‘fate map’ showing the orientation of prospective embryonic structures that emerge following gastrulation. aa–cc. Schematic organization of cell layers during early stages of development. aa. Blastula; bb. Blastocoel; cc. Gastrula.

Fig. 2. Schematic origin of radial and bilateral forms. The origin of phyletic diversity. Separate segments of cell layers meet at the opposite interior pole, where they join to emerge upward and out through the blastopore as tentacles (or, in the case of plants, a cylindrical shoot that opens in circlets of leaves or flowers.

Fig. 3. Schematic organogenesis. a. Blastula; b–f. Subductive gastrulation. The upper hemisphere of the blastula enters the interior at b, Reverses its trajectory, and draws both sides within the forming gastrula (c–f).
Fig. 8. Jaw formation. a–f. Gastrulation of somatic body and alimentary tract; g–k. Origin of the vertebrate jaw; l. Formation of teeth in the human jaw.

Fig. 9. Cardiovascular System. a. Blastula; b. Enlargement of endoderm layer; c. Separation of the artery and vein precursors; d-e. Onset of gastrulation; f–h. Reassembly of artery-vein configuration; i–k. Schematic depiction of heart formation; l. fully formed cardiovascular system.
Fig. 10. Origin of the nervous system. a–c. Separation of the afferent-efferent nerve primordia; d. Subductive gastrulation; e–g. Formation of the brain; h. Assembly of the afferent-efferent nerve pattern; i–l. Brain morphogenesis.

Fig. 11. Skull formation. a–d. Deformation of the upper hemisphere of the blastula resulting in formation of the skull (profile view); e–h. Closure of the ventral side by lateral compression (ventral view); i–m. Oblique view of the above.

Fig. 12. Formation of vertebrae, notochord, and nerve cord. a. Dorsal midline; b-c. Schematic cross-section of vertebra morphogenesis via subductive gastrulation. a and b. Formation of vertebrae; c. Enclosure of the notochord and nerve cord within the vertebrae.

Fig. 13. Formation of the brain and spinal column. Undulations in the membrane by compression prior to gastrulation induces the formation of spinal column elements.

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Fig. 15. Limb development. a–d. Ventral parting of limb girdle; e. Formation of archetypal primate (human) arm and leg; f. ‘South pole’ of blastula; g–i. Formation of sacrum; j. Segment of limb girdle; k. Distally directed displacement of sides; l–n. Formation of pelvis.

Fig. 20. Ovary, testis and urogenital tract origins. a–d. Bifurcation of gonad primordium; e–m. Parallel schematics showing similar morphogenesis of eye and gonads; n–p. Reproductive duct formation.
Fig. 22. Evolutionary origin of the bilateral body form by cellular ‘drift.’ a–i. Formation of blastula; j–n. Drift of apex to lateral position; o–y. Gastropod mollusk development, z–dd, Cephalopod mollusk development; ee–ii. Crustacean development; jj–nn. Arachnid development.

The concept of “embryo geometry” suggests that the vertebrate embryo might be produced by mechanical deformation of the blastula, a ball of cells formed when a fertilized egg splits. As these cells multiply, the volume and surface area of the ball expand, changing its shape. According to the hypothesis, the blastula preserves the geometry of the initial eight cells generated by the egg’s first three divisions, which establish the three axes of the vertebrate body.

The premise that complex animal form arises from mechanical forces acting on geometrically constrained populations of dividing cells in the early embryo provides a new lens through which to view developmental and evolutionary processes, and may pose a significant challenge to the Modern Synthesis’s dictum that evolution proceeds by a selection of adventitious mutations resulting from random mutations.

Though speculative, the model addresses the poignant absence in the literature of any plausible account of the origin of vertebrate morphology. A robust solution to the problem of morphogenesis—currently an elusive goal—will only emerge from consideration of both top-down (e.g., the mechanical constraints and geometric properties considered here) and bottom-up (e.g., molecular and mechano-chemical) influences.

Origin of the vertebrate body plan via mechanically biased conservation of regular geometrical patterns in the structure of the blastula, David B. Edelman, Mark McMenamin, Peter Sheesley, Stuart Pivar

Published: September 2016, Progress in Biophysics and Molecular Biology
DOI: 10.1016/j.pbiomolbio.2016.06.007

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