Molecular evidence for an activator–inhibitor mechanism in development of embryonic feather branching

124

The evolution of bilaterally symmetric feathers is a fundamental process leading toward flight. One major unsolved mystery is how the feathers of a single bird can form radially symmetric downy feathers and bilaterally symmetric flight feathers. In developing downy feather follicles, barb ridges are organized parallel to the long axis of the feather follicle. In developing flight-feather follicles, the barb ridges are organized helically toward the anterior region, leading to the fusion and creation of a rachis. Here we discover an anterior-posterior molecular gradient of wingless int (Wnt3)a in flight but not downy feathers. Global inhibition of the Wnt gradient transforms bilaterally symmetric feathers into radially symmetric feathers. Production of an ectopic local Wnt3a gradient reoriented barb ridges toward the source and created an ectopic rachis. We further show that the orientation of the Wnt3a gradient is dictated by the dermal papilla (DP). Swapping DPs between wing covert and breast downy feathers demonstrates that both feather symmetry and molecular gradients are in accord with the origin of the DP. Thus the fates of feather epidermal cells are not predetermined through some molecular codes but can be modulated. Together, our data suggest feathers are shaped by a DP3 Wnt gradient3helical barb ridge organization3creation of rachis3bilateral symmetry sequence. We speculate diverse feather forms can be achieved by adjusting the orientation and slope of molecular gradients, which then shape the topological arrangements of feather epithelia, thus linking molecular activities to organ forms and novel functions.axis determination ͉ dermal papilla ͉ evo-devo (evolution and development) ͉ morphogenesis ͉ skin appendages

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia

Yue

Jiang²,

Widelitz³

et al. 2006

124

“…The activator-inhibitor model of biological pattern formation has been applied to a wide range of developmental systems including those that generate periodic patterns, such as trichome formation on plant leaves, mammalian hair patterning, and feather branching in birds (21)(22)(23). It predicts the formation of concentration gradients of activator and inhibitor (1).…”

Section: Discussionmentioning

confidence: 99%

Genetic and cytological evidence that heterocyst patterning is regulated by inhibitor gradients that promote activator decay

Risser

Callahan

2009

111

The formation of a pattern of differentiated cells from a group of seemingly equivalent, undifferentiated cells is a central paradigm of developmental biology. Several species of filamentous cyanobacteria differentiate nitrogen-fixing heterocysts at regular intervals along unbranched filaments to form a periodic pattern of two distinct cell types. This patterning has been used to exemplify application of the activator-inhibitor model to periodic patterns in biology. The activator-inhibitor model proposes that activators and inhibitors of differentiation diffuse from source cells to form concentration gradients that in turn mediate patterning, but direct visualization of concentration gradients of activators and inhibitors has been difficult. Here we show that the periodic pattern of heterocysts produced by cyanobacteria relies on two inhibitors of heterocyst differentiation, PatS and HetN, in a manner consistent with the predictions of the activator-inhibitor model. Concentration gradients of the activator, HetR, were observed adjacent to heterocysts, the natural source of PatS and HetN, as well as adjacent to vegetative cells that were manipulated to overexpress a gene encoding either of the inhibitors. Gradients of HetR relied on posttranslational decay of HetR. Deletion of both patS and hetN genes prevented the formation of gradients of HetR, and a derivative of the inhibitors was shown to promote decay of HetR in a concentration-dependent manner. Our results provide strong support for application of the activator-inhibitor model to heterocyst patterning and, more generally, the formation of periodic patterns in biological systems.activator-inhibitor ͉ Anabaena ͉ development

“…These data extend previously documented roles for hedgehog signaling in dermal bone development (29,30) and suggest that this pathway plays an important role in polarizing dermal bone development along a proximal-distal axis. It is well established that hedgehog signaling is critical for the proper patterning and polarization of several organs in various animal taxa (32)(33)(34)(35)(36)(37), but here a similar role has been documented for bone development. The extent to which hedgehog-mediated outgrowth of other dermal bones (e.g., RA) has influenced species-specific differences in craniofacial shape would be a fruitful area of future investigation.…”

Section: Manipulation Of Hedgehog Pathway Signaling Affects Bone Devementioning

confidence: 99%

Craniofacial divergence and ongoing adaptation via the hedgehog pathway

Roberts

Albertson

et al. 2011

114

153

Adaptive variation in craniofacial structure contributes to resource specialization and speciation, but the genetic loci that underlie craniofacial adaptation remain unknown. Here we show that alleles of the hedgehog pathway receptor Patched1 (Ptch1) gene are responsible for adaptive variation in the shape of the lower jaw both within and among genera of Lake Malawi cichlid fish. The evolutionarily derived allele of Ptch1 reduces the length of the retroarticular (RA) process of the lower jaw, a change predicted to increase speed of jaw rotation for improved suction-feeding. The alternate allele is associated with a longer RA and a more robustly mineralized jaw, typical of species that use a biting mode of feeding. Genera with the most divergent feeding morphologies are nearly fixed for different Ptch1 alleles, whereas species with intermediate morphologies still segregate variation at Ptch1. Thus, the same alleles that help to define macroevolutionary divergence among genera also contribute to microevolutionary fine-tuning of adaptive traits within some species. Variability of craniofacial morphology mediated by Ptch1 polymorphism has likely contributed to niche partitioning and ecological speciation of these fishes.T he astounding diversity of vertebrate craniofacial morphology reflects adaptation to a wide variety of resources and environments. Evolution of craniofacial structure has been key to niche specialization and speciation in vertebrates (1), most famously exemplified by the varied beak morphology of Darwin's finches (2). The radiation of finches demonstrates both speciesdefining craniofacial divergence (2) and rapid adaptation of craniofacial morphology within species over the course of a few years in response to changes in resource availability (3). Although shifts in the expression of key craniofacial genes have been correlated with differences in trophic morphology among species of birds and cichlid fishes (4-8), the specific genetic loci producing these differences remain uncharacterized. As a result, it is not clear whether interspecific divergence and intraspecific adaptation share the same molecular genetic basis.