Abstract
Segmented animals are found in major clades as phylogenetically distant as vertebrates and arthropods. Typically, segments form sequentially in what has been thought to be a regular process, relying on a segmentation clock to pattern budding segments and posterior mitosis to generate axial elongation. Here we show that segmentation in Tribolium has phases of variable periodicity during which segments are added at different rates. Furthermore, elongation during a period of rapid posterior segment addition is driven by high rates of cell rearrangement, demonstrated by differential fates of marked anterior and posterior blastoderm cells. A computational model of this period successfully reproduces elongation through cell rearrangement in the absence of cell division. Unlike current models of steady-state sequential segmentation and elongation from a proliferative growth zone, our results indicate that cell behaviours are dynamic and variable, corresponding to differences in segmentation rate and giving rise to morphologically distinct regions of the embryo.
Highlights
Segmented animals are found in major clades as phylogenetically distant as vertebrates and arthropods
Sequential segmentation has been studied most extensively in vertebrates, where it relies on regulatory interactions between a segmentation clock that oscillates in the posterior growth zone and a posteriorly moving wavefront that stabilizes the readout of the clock to produce segments[1,2,3]
While we do not attempt to model the mechanisms leading to cell rearrangements or claim that cell rearrangements in the simulation exactly reflect those in the actual embryo, the simulation is consistent with a model in which cell rearrangements rather than a highly proliferative posterior growth zone drive axial elongation
Summary
Segmented animals are found in major clades as phylogenetically distant as vertebrates and arthropods. Cell rearrangements have been documented and implicated in elongation: high resolution live imaging in early Tribolium germbands shows that cells in the anterior germband intercalate during elongation[40] and that cells in the early growth zone move posteriorly, towards the midline[14,39,40] These local behaviours have not yet been explicitly linked quantitatively to germband elongation, during later stages. The transition from early segmentation, which gives rise to less elongated clones, to the more rapid later segmentation, which gives rise to more elongated clones, roughly coincides with the morphological thoracic/abdominal transition This suggests that distinct mechanisms may drive elongation in these two different regions of the embryo, with cell rearrangements being the primary driver of elongation during abdominal segmentation. We support this hypothesis with a computational model of elongation during posterior segmentation that is created solely by cell rearrangements
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