Retinoic acid influences the timing and scaling of avian wing development

Abstract

Summary A fundamental question in biology is how embryonic development is timed between different species. To address this problem, we compared wing development in the quail and the larger chick. We reveal that pattern formation is faster in the quail as determined by the earlier activation of 5′ Hox genes, termination of developmental organizers ( Shh and Fgf8 ), and the laying down of the skeleton ( Sox9 ). Using interspecies tissue grafts, we show that developmental timing can be reset during a critical window of retinoic acid signaling. Accordingly, extending the duration of retinoic acid signaling switches developmental timing between the quail and the chick and the chick and the larger turkey. However, the incremental growth rate is comparable between all three species, suggesting that the pace of development primarily governs differences in the expansion of the skeletal pattern. The widespread distribution of retinoic acid could coordinate developmental timing throughout the embryo.

The forelimbs of Alvarezsauroidea (Dinosauria: Theropoda): Insight from evolutionary teratology

“…As another possibility, it should be noted that similar growth rates may ultimately produce proportionally variable forelimbs. Among current avian species, developmental temporality is faster in quail than in chicken but independent of growth rate, which is equivalent between the two species (Stainton & Towers, 2022).…”

Fgf signalling triggers an intrinsic mesodermal timer that determines the duration of limb patterning

“…In this model, Meis levels need to be low enough to allow the transition from stylopod to zeugopod specification (Figure 8). Indeed, the level of RA signalling correlates with-and can change the rate of-5' Hox activation between different avian species 17 .…”

“…The loss of RA signalling in the distal part of the limb allows the initiation of the late distal patterning phase (light blue in Figure 1a) that coincides with Hoxa/d13 gene activation 11,18 , which specifies the positional values of the autopod 19 (wrist and digits). In the quail, chick and turkey, the late patterning phase runs for a similar duration and takes between 48 and 54 h 17 .…”

“…Prolonging RA signalling in quail and chick wings extends the early patterning phase, and because the late phase remains unchanged, the duration of patterning is then equivalent to that of chick and turkey wings, respectively 17 . It is likely that the degradation of RA and/or its transcriptional effectors (Meis1/2) is responsible for species' differences in the duration of patterning.…”

“…The depletion of RA is influenced by growth of the limb away from the body and by the degradation enzyme, Cyp26b1, which is transcriptionally induced by opposing Fgf signals from the apical ectodermal ridge 15, 16 (AER-Fgfs – the AER is a thickening of the distal epithelium – Figure 1a). In different avian species (quail, chick and turkey), the duration of the early proximal patterning phase varies and takes between 12 and 30h 17 . The loss of RA signalling in the distal part of the limb allows the initiation of the late distal patterning phase (light blue in Figure 1a) that coincides with Hoxa/d13 gene activation 11, 18 , which specifies the positional values of the autopod 19 (wrist and digits).…”