How did the first feathers grow?

Friends who don't usually pay attention to dinosaurs must have noticed that dinosaurs have started to grow hair. When we were young, dinosaurs were always seen as cold-blooded and ferocious, wearing armor. Now that dinosaurs have grown feathers, especially those small dinosaurs covered with feathers, they have become docile and cute, and you can't help but want to touch them. What's the reason for the 180-degree turn in the image of dinosaurs? How did the first tuft of feathers grow?

Dinosaurs are now covered in feathers in movies, TV shows and video games

Written by Yang Zixiao (University College Cork, Ireland)

You must have picked up beautiful feathers before! Feathers are light and resilient, seemingly simple in structure but very delicate, with a variety of colors, and some even have magical patterns (see the picture below). Who wouldn’t want to hold one in their hands and play with it?

Figure 1. A blue peacock, Pavo cristatus, spreading its feathers. Source:
https://en.wikipedia.org/wiki/Peafowl

This impulse to collect feathers can be traced back to prehistoric humans. More than 40,000 years ago, Neanderthals began to collect large feathers from bird wings to decorate themselves or use in certain rituals [1]. In the subsequent development of human civilization, feathers have always been a very important element and can be seen in many aspects such as religion, culture, art, fashion, science, etc. (see the picture below).

Figure 2. A feathered war headdress worn by a 19th-century Indian chief (left; Cincinnati Art Museum) and Darwin’s book The Descent of Man and Sexual Selection (right): Inspired by the exaggerated feathers of male birds, Darwin proposed a theory of evolution through sexual selection.

So, it is no wonder that when the first feathered dinosaur fossil was unveiled on October 18, 1996 (see the picture below), it caused a huge sensation and many people were "shocked" [2]. The next day after the fossil was unveiled, the New York Times reported it in detail on the front page with the title "Feathery Fossil Hints Dinosaur-Bird Link" [3]. This historic dinosaur specimen was discovered in Northeast my country and was named Sinosauropteryx prima [4].

Figure 3. The holotype of Sinosauropteryx prima (left; Chen et al., 1998[4]) and an artistic conception created by Professor Zhao Chuang (right).

There was a first, then a second, and a third. In the following three decades, thousands of feathered animal fossils have been found in northeast my country, including Anchiornis huxleyi, a restored model of which was recently presented to the French president as a state gift (see the picture below).

Figure 4. Artistic reconstruction of Anchiornis huxleyi (by Michael DiGiorgio).

These ancient feathers are like pages in a book, recording the evolution of feathers over millions of years. Through them, we know that feathers have ancient origins: they appear not only in birds and dinosaurs, but also in the dinosaurs’ cousins, pterosaurs[5]. Feathers in the past were also more diverse (see figure below), and modern birds have only inherited a subset of feather types[6].

Figure 5. Seven types of feather structures in modern birds (above) and 12 types of feather structures found in fossils (below). Source: Benton et al., 2019[6]

Feathers were not originally used for flying. Compared to modern bird feathers, early feathers were very simple in structure and were very limited in distribution, so feathers were probably used for display[7] or feeling (similar to beards)[8]. In addition, scientists have discovered that some pterosaurs had dense feathers on their bodies, which may have played a major role in keeping warm[5].

Despite these important discoveries of feather fossils, our understanding of feather evolution is far from complete. In fact, feather fossils only record half of the story of feather evolution - the other half is hidden in the skin.

The other half of the story

Scientists have long realized that feathers evolved from reptile scales. At first glance, this process seems simple, just replace the scales with feathers, right? In fact, it is not: compared with reptiles, the feathers of modern birds have a series of complex skin structures closely related to them.

During bird development, depressions and folds form in genetically specified areas of the skin, forming hair follicles that control the distribution and growth of feathers. Fine muscle and nerve tissue also develop around the hair follicles (see figure below) to sense and control the spatial position of each feather[9].

Figure 6. The fine structure of a bird feather follicle. Source: Lucas and Stettenheim, 1972[9]

Feather follicles are also home to many pigment cells that deliver pigment to growing feathers. By controlling the timing and type of pigment delivered, birds can “print” different feather colors and patterns from top to bottom on their skin [10] (see figure below).

Figure 7. The formation of bird feather color. Left: As feathers grow, melanocytes in the hair follicles are activated and deliver pigment to the growing feathers. Right: The growth process of Plymouth Rock chicken feathers; note the order in which the feathers are “printed” from top to bottom. Source: Lin et al., 2013[10]

In addition, compared to the “armor” of reptiles, bird skin is thinner and softer, creating the necessary conditions for subtle skin movements such as erecting feathers and flexible flapping of wings[9].

So, as feathers evolved, skin also underwent radical changes. So how did this happen?

Just like feather fossils, skin can also be preserved in fossils. Scientists have found skin fossils from some early birds and their dinosaur relatives, and these fossils even preserve exquisite cellular structures [11] (see figure below).

Figure 8. Fossilized skin cells of Confuciusornis. Source: McNamara et al., 2018[11]

However, by comparing them with modern birds, scientists have found that the skin of early birds and their dinosaur relatives was already very “modern” [11]. Therefore, to understand the evolution of skin structure, we need to go down the evolutionary tree and look for clues in the dinosaur groups that branched earlier.

New fossils, new clues

On May 21, 2024, we published a new study in Nature Communications [12], which made important progress in deciphering the mystery of skin and feather evolution: although some dinosaurs evolved early feathers, their skin structure did not change in the parts of their bodies where there were no feathers, and was almost exactly the same as the scaly skin of modern reptiles.

The clue comes from a new specimen of Psittacosaurus, also found in northeast my country. As the name suggests, the most prominent feature of Psittacosaurus is its parrot-like mouth (pictured below). Equally striking is its tail: a row of very simple early feathers grow neatly on the back of its tail.

Figure 9. Artistic reconstruction of Psittacosaurus. Gabriel N. Ugueto

Although the Psittacosaurus lived in the early Cretaceous period (about 120 million years ago), it was a type of dinosaur that branched off very early on the dinosaur evolutionary tree: the dinosaur group it belonged to (ornithischian dinosaurs) parted ways with other dinosaurs and evolved in different directions in the Triassic period (about 240 million years ago).

Amazingly, the fossilized skin in our specimen is invisible to the naked eye. Only when you hold up an ultraviolet light—yes, the kind you use to check banknotes—does the scaly skin become visible, fluorescing a faint orange-yellow color in the dark (below).

Figure 10. New specimen of Psittacosaurus under natural light (above) and ultraviolet light (below) | Photo provided by the author

This fluorescence does not come from the skin itself. The original skin structure is replicated during the fossilization process by silica minerals, which fluoresce when excited by ultraviolet light. Bones (above) also fluoresce, but the mineral composition (calcium phosphate) is different from that of fossilized skin, so they have a different fluorescent color.

What is even more amazing is the exquisite preservation of the skin fossils. Many fine skin structures (pictured below) are perfectly reproduced by minerals, preserving the epidermis (including stratum corneum and non-stratum corneum), keratinocytes, and very tiny skin pigments (melanosomes) that are 2,000 times smaller than a grain of sand.

Figure 11. The epidermis (A–B), keratinocytes (A–B) and melanosomes (C–D) of the skin preserved in the fossil of Psittacosaurus.

The keratinocytes of the fossil skin are highly consistent with those of modern reptiles in shape and size. At the same time, the keratinocytes in the fossil also partially fuse with the adjacent cells on the side to form a layer (below) - this cell fusion phenomenon only occurs between the keratinocytes of reptiles.

Figure 12. The structure of the corneocyte layer of Psittacosaurus (top; provided by the author) is consistent with that of the corneocyte layer of crocodiles (bottom; Szewczyk and Stachewicz, 2020[13]).

The distribution of pigments in fossil skin is exactly the same as that of modern crocodiles: pigments are either absent, only present in the lower layer of the epidermis (non-cuticle), or present in both the upper and lower layers of the epidermis (cuticle and non-cuticle). In crocodile scales, these three distributions correspond to white, intermediate colors (gray), and black, forming dotted or striped patterns on the body.[14] Therefore, the skin of Psittacosaurus is likely to have some light and dark patterns.

This is obviously different from the distribution of skin pigments in birds. After the birds have feathers, the pigment cells in the epidermis of birds are concentrated in the hair follicles and transport the generated pigments to the feathers, while the epidermis itself has very little pigment distribution, so it looks pink. The black chicken is a special case derived from the process of bird evolution. Due to some genetic changes, the black chicken has a large number of pigment cells and pigments in the dermis below the epidermis, while its epidermis, like other birds, has very little pigment distribution [15] (see figure below).

Figure 13. Black skin (A, C) and pink skin (B, D) of birds; e, epidermis; m, melanin. Source: Nicolaï et al., 2020[15]

In terms of skin thickness, we found that the skin on the belly of Psittacosaurus was thinner than that of modern reptiles, but this just shows that the two are the same in composition. The armor-like scaly skin of reptiles is due to the abundance of corneous beta proteins in it. There is no such protein in the soft skin of birds - like our mammal skin, the soft skin of birds is made of alpha keratin. Birds and mammals do not need very tough skin because they are protected by feathers and hair. But Psittacosaurus is different. Its thin belly can only be tough enough to achieve the function of physical protection if it is rich in beta keratin.

The scales on bird legs and claws are very similar to those of reptiles, and are also rich in β-keratin. However, scientists have discovered that bird scales are secondary: after the evolution from scales to feathers, some of the bird feathers evolved into scales again (see figure below) [16, 17].

Figure 14. The evolution of theropod dinosaurs (including birds) saw the gradual transformation of hindlimb feathers into scales. Source: Zheng et al., 2013[17]

Why is the skin on the belly of a Psittacosaurus thinner than that of modern reptiles? Does it feel soft? This may be because the daily posture of a Psittacosaurus is different from that of reptiles. When a Psittacosaurus was young, it walked on four legs. As it grew up, its forelimbs gradually became shorter than its hind limbs, and it gradually became a bipedal walker (see the picture below). Judging from the proportions of the forelimbs and hind limbs, the Psittacosaurus we studied should have started walking on two legs.

Figure 15. A family of Psittacosaurus: the young ones walk on four legs, the older ones walk on two legs. | Drawing by Bob Nicholls

After walking on two legs, the belly was lifted off the ground, away from the gravel and plants on the ground. Therefore, compared with quadrupedal reptiles, the belly of the Psittacosaurus did not need thick armor to protect it.

Although our specimen does not preserve any skin in the tail, since Psittacosaurus had feathers on its tail, the corresponding skin locations should have developed some bird-like skin features.

Based on all the clues above, the skin of Psittacosaurus developed in two different ways: reptilian skin developed in bare (featherless) areas, and bird-like skin developed in feathered areas.

This skin development feature reflects the regional expression of genes. This phenomenon can also be seen in the skin development process of modern birds: some genes are responsible for "spatial planning", specifying where feathers will grow and where they will not; in the planned area, the genes responsible for forming feathers and skin begin to express, and eventually different feather and skin structures develop in different body regions. Pigeons can even achieve the arbitrary transformation of feathers and scales on their feet by changing the genes responsible for "spatial planning" [18] (see figure below).

Figure 16. Two "spatial planning" genes of pigeons, Pitx1 and Tbx5. Pitx1 specifies the area of ​​the hind limbs, and Tbx5 specifies the area of ​​the forelimbs. The color depth indicates the expression level of the corresponding gene in the feet; when Pitx1 expression is weak and Tbx5 expression is strong, the skin on the feet will grow more like the skin on the forelimbs and be covered with feathers. | Image source: Domyan et al., 2016[18]

This gene regulation mechanism of birds should have appeared in Psittacosaurus. Through some genes, the growth positions of feathers and scales were planned in advance. Psittacosaurus grew feathers and bird-like skin on the back of its tail, and reptile-like scaly skin in other places.

This regional skin development strategy of the Psittacosaurus may have played a decisive role in the early evolution of feathers. Maintaining the original state of reptile ancestors in places where feathers do not grow can ensure that the physiological functions of the skin - physical protection, water retention, immunity, etc. - still function normally as before. In this way, when trying to grow the first tuft of feathers, these animals can survive in nature, thus passing on precious feather genes to the next generation and to today's birds (pictured below).

Figure 17. “Don’t forget who you are!” | Source:
https://twitter.com/hmns/status/1757052320813117512/photo/1

References

[1] Peresani, M., Fiore, I., Gala, M., Romandini, M. & Tagliacozzo, A. Late Neandertals and the intentional removal of feathers as evidenced from bird bone taphonomy at Fumane Cave 44 ky BP, Italy. Proc. Natl Acad. Sci. USA 108, 3888–3893 (2011).

[2] Padian, K. 25th anniversary of the first known feathered dinosaurs. Nature 613, 251–252 (2023).

[3] Browne, MW Feathery fossil hints dinosaur-bird link. The New York Times, 1 (1996).

[4] Chen, PJ, Dong, ZM & Zhen, SN, 1998. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391, 147–152 (1998).

[5] Yang, Z. et al. Pterosaur integumentary structures with complex feather-like branching. Nat. Ecol. Evol. 3, 24–30 (2019).

[6] Benton, MJ, Dhouailly, D., Jiang, B. & McNamara, M. The early origin of feathers. Trends Ecol. Evol. 34, 856–869 (2019).

[7] Mayr, G., Pittman, M., Saitta, E., Kaye, TG & Vinther, J. Structure and homology of Psittacosaurus tail bristles. Palaeontology 59, 793–802 (2016).

[8] Persons IV, WS & Currie, PJ Bristles before down: a new perspective on the functional origin of feathers. Evolution 69, 857–862 (2015).

[9] Lucas, AM & Stettenheim, PR Avian Anatomy. Integument, Parts I and II (US Government Printing Office, 1972)

[10] Lin, SJ et al. Topology of feather melanocyte progenitor niche allows complex pigment patterns to emerge. Science 340, 1442–1445 (2013).

[11] McNamara, ME et al. Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds. Nat. Commun. 9, 2072 (2018).

[12] Yang, ZX, Jiang, BY, Xu, JX & McNamara, ME Cellular structure of dinosaur scales reveals retention of reptile-type skin during the evolutionary transition to feathers. Nat. Commun. 15, 4063 (2024).

[13] Szewczyk, PK & Stachewicz, U. Collagen fibers in crocodile skin and teeth: A morphological comparison using light and scanning electron microscopy. J. Bionic Eng. 17, 669–676 (2020).

[14] Alibardi, L. Histology, ultrastructure, and pigmentation in the horny scales of growing crocodilians. Acta Zool. 92, 187–200 (2011).

[15] Nicolaï, MP, Shawkey, MD, Porchetta, S., Claus, R. & D'Alba, L Exposure to UV radiance predicts repeated evolution of concealed black skin in birds. Nat. commun. 11, 2414 (2020).

[16] Wu, P., Lai, YC, Widelitz, R. & Chuong, CM Comprehensive molecular and cellular studies suggest avian scutate scales are secondarily derived from feathers, and more distant from reptilian scales. Sci. Rep. 8, 16766 (2018).

[17] Zheng, XT et al. Hind wings in basal birds and the evolution of leg feathers. Science 339, 1309-1312 (2013).

[18] Domyan, ET et al. Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species. eLife 5, p.e12115 (2016).

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