Crocodile Head Scales Are Not Developmental Units But Emerge from Physical Cracking

Using computer graphics and developmental biology techniques, Milinkovitch et al. show that the scales on the face and jaws of crocodilians are not genetically controlled developmental units and that their spatial patterning is generated through physical cracking of the skin. [CREDIT: Michel C. Milinkovitch & Adrien Debry]
Head scales in many snakes (here, a corn snake) and lizards are polygons with stereotyped spatial distribution: The left (yellow) and right (red) scale edges overlap when reflected across the sagittal symmetry plane (blue). [CREDIT: Liana Manukyan & Michel C. Milinkovitch]
On the other hand, polygonal scales on the face and jaws of Nile crocodiles have a largely random spatial distribution without symmetrical correspondence between left (yellow) and right (red). [CREDIT: Liana Manukyan & Michel C. Milinkovitch]
Similarly, scales from different crocodile individuals have different distributions of sizes and localizations (blue and red edges from top and bottom crocodiles, respectively). [CREDIT: Liana Manukyan & Michel C. Milinkovitch]
In snakes and lizards, each body scale differentiates from a primordium (in situ hybridization with Shh gene probe), and head scales also develop from primordia, with positional cues determining scale identity. [CREDIT: Nicolas Di-Poi & Liana Manukyan]
Similarly, postcranial scales (right = zoom on trunk) in crocodiles also develop from primordia (Ctnnb1 probe) that differentiate into symmetrical then oriented asymmetrical overlapping scales. [CREDIT: Nicolas Di-Poi]
Crocodile head scales never form scale primordia but instead develop a pattern of sensory organs that detect surface pressure waves [inset detail; dermal pressure receptors (DPRs)] before any scale appears (probe: Ctnnb1). [CREDIT: Nicolas Di-Poi & Michel C. Milinkovitch]
Starting about 55 days after oviposition (E55), grooves progressively appear, propagate and interconnect (while avoiding DPRs) to form a continuous network across the developing skin. [CREDIT: Nicolas Di-Poi & Michel C. Milinkovitch]
Skin sections (left) indicate that cracks correspond to epidermal bulges that reach the stiff underlying tissues. Immunohistochemnistry (right) indicates increased cell proliferation (green) within the skin grooves corresponding to cracks. Abbreviations: primary (pc) and secondary (sc) cracks (ep, epidermis, de, dermis, bo, bone tissue). [CREDIT: Nicolas Di-Poi]
his process is analogous to true physical cracking of a shrinking material layer adherent to a nonshrinking substrate, as in drying or cooling pavement. [CREDIT: Michel C. Milinkovitch]
Other cases of physical cracking are drying mud (left), cooling ceramics (top right), and drying adhesive plastic sheets (bottom right). [CREDIT: Liana and Heorhiy Manukyan & Michel C. Milinkovitch]
However, in crocodiles, it is not the cracking layer that shrinks but the underlying substrate layer (the embryonic skull) that grows, hence generating the mechanical stress that causes the skin to crack. [CREDIT: Michel C. Milinkovitch & Adrien Debry]
Therefore, scales on the face and jaws of crocodiles (i) are not serial homologs of scales elsewhere on the body, (ii) are not even genetically controlled developmental units. Instead, they emerge from physical cracking. [CREDIT: Michel C. Milinkovitch]