Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

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.

Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus

“…Specifically, many questions remain regarding the cellular aspects of this process, which takes place in a very different tissue environment compared with Drosophila (Peel et al, 2005). The role of cell proliferation and migration in the formation of segments from the growth zone varies among species and modes of segmentation (Beermann et al, 2011; Chipman, 2008; Copf et al, 2004; McGregor et al, 2009; Nakamoto et al, 2015; Oberhofer et al, 2014; Peel et al, 2005; Ten Tusscher, 2013). Whereas some require intensive cell proliferation [e.g.…”

Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum

“…As germ band extension requires the coordination of the amnion with the embryo, extracellular signaling is likely to be important in regulating cellular rearrangements in both tissues (e.g. Nakamoto et al, 2015).…”

Hexapoda: Comparative Aspects of Early Development

“…Similarly, it is obvious from an observation of embryos of most insect species that during axis elongation the germband becomes narrower and the growth zone changes from having a rounded shape and being wider than the germband to becoming narrow and pointed, suggesting signifi cant cell movements. However, this has not been quantifi ed clearly (Nakamoto et al 2015 ).…”