Provocative new ideas regarding morphological complexity have emerged from comparative genomic studies. It is now clear that the genomes of primitive animals, which do not form organs, "...include many of the genes responsible for guiding development of other animals' complex shapes and organs" (Pennisi, 2008). Thus, developmentally simple animals possess the same molecular genetic circuits that vertebrates use to make complex body parts. This unexpected realization prompts the obvious question - If genomic complexity is not the underpinning of vertebrate organogenesis - What is? We hypothesize that tissues and organs arise from emergent biophysical and biomechanical processes that comprise a biomechanical morphogenetic code.To study morphogenetic forces we use computational time-lapse imaging to capture cellular displacements and tissue motion during gastrulation and the formation of the primary vascular network. Engineering approaches and statistical physics allow computation of tissue displacements using the motion of ECM fibrils as in situ markers for passive motion, while simultaneously tracking, individual, total cellular displacement(s). This approach allows calculation of active cellular autonomous motility (locomotion) versus passive convective tissue motion. The data demonstrate that passive tissue motion is responsible for much of what has heretofore been termed "migration". Our work has important implications for understanding cellular guidance mechanisms and chemotactic gradients purported to drive morphogenesis at early stages of amniote embryogenesis.

Supported by the G. Harold and Leila Y. Mathers Charitable Foundation (CDL, BJR and AC); NIHLB R01 068855 (CDL) and NIHLB R01 085694 (BJR); Hungarian Research Fund OTKA T047055, American Heart Association Scientist Development grant 0535245N and NIHLB R01 HL087136 (to A. C.).

Ancient animals arose from unicellular organisms that were the product of billions of years of prior evolution. In this talk I will consider the role played by a core set of "dynamical patterning modules" (DPMs) in the origination, development and evolution of multicellular animals, the Metazoa. These functional modules consist of the products of certain genes of the "developmental-genetic toolkit" (e.g., cadherins, Notch and Wnt pathway, Hh, BMP and FGF; chitin, collagen) in association with physical processes and effects characteristic of chemically and mechanically excitable systems of the "mesoscale" (i.e., linear dimension ~0.1-10 mm). Once cellular life achieved this spatial scale by the most basic DPM, cell-cell adhesion, a variety of physical forces and effects came into play, including cohesion, viscoelasticity, diffusion, spatiotemporal heterogeneity based on lateral inhibition, and global synchronization of oscillatory dynamics. I will show how toolkit gene products and pathways that pre-existed the Metazoa acquired novel morphogenetic functions simply by virtue of the change in scale and context inherent to multicellularity, ultimately becoming integrated into developmental programs. This perspective helps explain the Cambrian explosion and the apparent paradox in which divergent modern animal types utilize the same molecular toolkit for embryogenesis.

Evolution by natural selection requires three steps. New variants of organisms: must arise, must have an impact on fitness (survival or fecundity), and must (ultimately) be heritable. The first step - how new variants arise - remains controversial. Traditionally, new phenotypes are attributed to novel genotypes (mutants or recombinants). But developmental plasticity - the same genotype yields different forms in different environments - may be a more important source of new variants than generally recognized. The absence of heritable variation for direction of asymmetry in species that show a random mixture of asymmetric forms (i.e., equal numbers of right- and left-handed forms), identifies a unique phenotype - 'direction of asymmetry' - for which there is no genotype. A wide-ranging survey of asymmetry variation within and among species of animals and plants offers some of the strongest evidence to date for a 'phenotype-precedes-genotype' mode of evolution. In addition, the tendency of many animals to learn (e.g., handed behavior) may facilitate both the origin and the amplification of right-left morphological differences via developmental plasticity. Such an interplay between learning and developmental plasticity might greatly enhance the rate of morphological evolution.