Embryonic bauplans and the developmental origins of facial diversity and constraint

Abstract

A central issue in biology concerns the presence, timing and nature of phylotypic periods of development, but whether, when and why species exhibit conserved morphologies remains unresolved. Here, we construct a developmental morphospace to show that amniote faces share a period of reduced shape variance and convergent growth trajectories from prominence formation through fusion, after which phenotypic diversity sharply increases. We predict in silico the phenotypic outcomes of unoccupied morphospaces and experimentally validate in vivo that observed convergence is not due to developmental limits on variation but instead from selection against novel trajectories that result in maladaptive facial clefts. These results illustrate how epigenetic factors such as organismal geometry and shape impact facial morphogenesis and alter the locus of adaptive selection to variation in later developmental events.

What limits the morphological disparity of clades?

“…For this and other reasons, conventional discrete character morphospacesand the estimates of disparity derived from them-may not be best suited for recognizing the changes of deepest developmental and evolutionary significance. Morphospaces that take account of the developmental depth of characters have long been called for [3], and some moves have been made towards realizing these for particular clades [48,[183][184][185][186]. Several authors have distinguished between intrinsic and extrinsic limits to disparity [7], with intrinsic factors being those that operate within the individuals and lineages that constitute a clade (broadly equating to geometric and developmental constraints) and extrinsic or ecological factors being those imposed from the outside (biological and physical restrictions) [6,26].…”

A dynamic Shh expression pattern, regulated by SHH and BMP signaling, coordinates fusion of primordia in the amniote face

“…We have shown in a large comparative analysis of the development of the amniote face that a phylotypic stage exists around the time of palatal fusion (Young et al, 2014). At this time, facial shapes among amniotes converge in order for the primary palate to form, and after that, the faces are able to diverge into the array of morphologies present in adult amniotes.…”

“…The globular process of the FNP and the lower margins of the nasal pits next meet at the distal tip of the MxP, an event associated with subsequent fusion of the prominences. After fusion, the avian FNP undergoes rapid expansion, associated with the derived proportions of the premaxilla and upper beak (Young et al, 2014).…”

“…We performed a 3D morphometric analysis of facial shape changes during primary palate morphogenesis in the chicken. We applied homologous landmarks (n=20) to the embryonic craniofacial region (Young et al, 2014), performed a Procrustes superimposition to remove the effects of scale and orientation, and regressed the individual (n=17) shape coordinates against developmental age (hours of incubation) (r 2 =0.919, explaining 81.1% total shape variation). To visualize shape changes associated with age, we next applied the associated shape-age vector to a representative 3D model of an early stage (84 h) embryo, and projected it to 160 h of development (i.e.…”

“…An important morphogenetic event in facial development is the fusion of the maxillary (MxP), lateral nasal (LNP) and medial nasal (MNP) portion of the frontonasal process (FNP) to form the primary palate of the upper jaw. We have recently determined that a phylotypic stage exists, precisely around the time of fusion of the facial primordia (Young et al, 2014). At this time, the faces of amniote embryos exhibit the highest degree of morphological resemblance because, independent of the final adult form, they all pass through a developmental stage in which the facial buds collide and fuse to form the face (Young et al, 2014).…”