Feathers play a crucial role in keeping birds warm, enabling flight, and allowing them to communicate. Scientists believe they evolved from simpler structures called proto-feathers, which were found in some dinosaurs. In our new study, published today in PLOS Biology, we found that blocking the Shh pathway temporarily disrupts feather formation, leading to simple, unbranched feather buds—similar to proto-feathers. However, this effect is not permanent. As the birds continue to develop before and after birth, their feathers gradually recover, and by adulthood, they have nearly full plumage. Our research shows that, unlike the scales on birds’ feet, the genetic network responsible for feather development is highly resilient. Even with significant genetic or environmental perturbations, feathers still form properly.
Feathers are among the most complex cutaneous appendages in the animal kingdom. While their evolutionary origin has been widely debated, our research, combined with paleontological discoveries and developmental biology studies, suggests that feathers evolved from simple structures known as proto-feathers. These primitive structures, composed of a single tubular filament, emerged around 200 million years ago in certain dinosaurs. Paleontologists continue to discuss the possibility of their even earlier presence in the common ancestor of dinosaurs and pterosaurs (the first flying vertebrates with membranous wings) around 240 million years ago.
Proto-feathers are simple, cylindrical filaments. They differ from modern feathers by the absence of barbs and barbules, and by the lack of a follicle—an invagination at their base. The emergence of proto-feathers likely marked the first key step in feather evolution, initially providing thermal insulation and ornamentation before being progressively modified under natural selection to give rise to the more complex structures that enabled flight.
Our laboratory studies the role of molecular signaling pathways (communication systems that transmit messages within and between cells), such as the Sonic Hedgehog (Shh) pathway, in the embryonic development of scales, hair, and feathers in modern vertebrates. In a previous study, we stimulated the Shh pathway by injecting an activating molecule into the blood vessels of chicken embryos and observed the complete and permanent transformation of scales into feathers on the bird’s feet (see Figure 1 below).
Figure 1: Over-activation of the Shh pathway triggers a complete and permanent transformation of reticulate foot scales into feathers, whereas Shh pathway inhibition temporarily produces unbranched and non-invaginated feather buds — akin to proto-feathers.
Recreating the first dinosaur proto-feathers
"Since the Shh pathway plays a crucial role in feather development, we wanted to observe what happens when it is inhibited," explains Rory Cooper, a postdoctoral researcher in our lab and co-author of the study. By injecting a molecule that blocks the Shh signaling pathway on the 9th day of embryonic development – just before feather buds appear on the wings – we observed the formation of unbranched and non-invaginated buds, resembling the putative early stages of proto-feathers.
"Our experiments show that while a transient disturbance in the development of foot scales can permanently turn them into feathers, it is much harder to permanently disrupt feather development itself", concludes Michel Milinkovitch. Clearly, over the course of evolution, the network of interacting genes has become extremely robust, ensuring the proper development of feathers even under substantial genetic or environmental perturbations. The big challenge now is to understand how genetic interactions evolve to allow for the emergence of morphological novelties such as proto-feathers (see Figure 2 below).
Figure 2: Embryos treated with sonidegib, a potent inhibitor of the Shh pathway, at the 9th day of incubation exhibit feather buds with no feather barbs and no follicle invagination.
Much additional information is available in the original article:
In vivo sonic hedgehog pathway antagonism temporarily results in ancestral proto-feather-like structures in the chicken
Rory L. Cooper, Michel C. Milinkovitch
PLoS Biol 23(3): e3003061. https://doi.org/10.1371/journal.pbio.3003061