Active shape programming drives Drosophila wing disc eversion

How complex 3D tissue shape emerges during animal development remains an
important open question in biology and biophysics. In this work, we study
eversion of the Drosophila wing disc pouch, a 3D morphogenesis step when
the epithelium transforms from a radially symmetric dome into a curved
fold shape via an unknown mechanism. To explain this morphogenesis, we
take inspiration from inanimate ”shape-programmable” materials, which are
capable of undergoing blueprinted 3D shape transformations arising from
in-plane gradients of spontaneous strains. Here, we show that active,
in-plane cellular behaviors can similarly create spontaneous strains that
drive 3D tissue shape change and that the wing disc pouch is shaped in
this way. We map cellular behaviors in the wing disc pouch by developing a
method for quantifying spatial patterns of cell behaviors on arbitrary 3D
tissue surfaces using cellular topology. We use a physical
shape-programmability model to show that spontaneous strains arising from
measured active cell behaviors create the tissue shape changes observed
during eversion. We validate our findings using a knockdown of the
mechanosensitive molecular motor MyoVI, which we find to reduce active
cell rearrangements and disrupt wing pouch eversion. This work shows that
shape programming is a mechanism for animal tissue morphogenesis and
suggests that there exist intricate patterns in nature that could present
novel designs for shape-programmable materials.