Species Tailoured Contribution of Volumetric Growth and Tissue Convergence to Posterior Body Elongation in Vertebrates

Abstract

Axial elongation is a widespread mechanism propelling the generation of the metazoan body plan. A widely accepted model is that of posterior growth, where new tissue is continually added from the posterior unsegmented tip of the body axis. A key question is whether or not such a posterior growth zone generates sufficient additional tissue volume to generate elongation of the body axis, and the degree to which this is balanced with tissue convergence and/or growth in already segmented regions of the body axis. We applied a multi-scalar morphometric analysis during posterior axis elongation in zebrafish. Importantly, by labelling of specific regions/tissues and tracking their deformation, we observed that the unsegmented region does not generate additional tissue volume at the caudal tip. Instead, it contributes to axis elongation by extensive tissue deformation at constant volume. We show that volumetric growth occurs in the segmented portion of the axis and can be attributed to an increase in the size and length of the spinal cord and notochord. FGF inhibition blocks tissue convergence within the tailbud and unsegmented region rather than affecting volumetric growth, showing that a conserved molecular mechanism can control convergent morphogenesis, even if by different cell behaviours. Finally, a comparative morphometric analysis in lamprey, dogfish, zebrafish and mouse reveal a differential contribution of volumetric growth that is linked to a switch between external and internal modes of development. We propose that posterior growth is not a conserved mechanism to drive axis elongation in vertebrates. It is instead associated with an overall increase in growth characteristic of internally developing embryos that undergo embryonic development concomitantly with an increase in energy supply from the female parent.