Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2004;48(2-3):249-70.
doi: 10.1387/ijdb.041825pw.

Evo-Devo of amniote integuments and appendages

Ping Wu  1 , Lianhai Hou, Maksim Plikus, Michael Hughes, Jeffrey Scehnet, Sanong Suksaweang, Randall Widelitz, Ting-Xin Jiang, Cheng-Ming Chuong
Affiliations
Review

Evo-Devo of amniote integuments and appendages

Ping Wu et al. Int J Dev Biol. 2004.

Abstract

Integuments form the boundary between an organism and the environment. The evolution of novel developmental mechanisms in integuments and appendages allows animals to live in diverse ecological environments. Here we focus on amniotes. The major achievement for reptile skin is an adaptation to the land with the formation of a successful barrier. The stratum corneum enables this barrier to prevent water loss from the skin and allowed amphibian / reptile ancestors to go onto the land. Overlapping scales and production of beta-keratins provide strong protection. Epidermal invagination led to the formation of avian feather and mammalian hair follicles in the dermis. Both adopted a proximal - distal growth mode which maintains endothermy. Feathers form hierarchical branches which produce the vane that makes flight possible. Recent discoveries of feathered dinosaurs in China inspire new thinking on the origin of feathers. In the laboratory, epithelial - mesenchymal recombinations and molecular mis-expressions were carried out to test the plasticity of epithelial organ formation. We review the work on the transformation of scales into feathers, conversion between barbs and rachis and the production of "chicken teeth". In mammals, tilting the balance of the BMP pathway in K14 noggin transgenic mice alters the number, size and phenotypes of different ectodermal organs, making investigators rethink the distinction between morpho-regulation and pathological changes. Models on the evolution of feathers and hairs from reptile integuments are discussed. A hypothetical Evo-Devo space where diverse integument appendages can be placed according to complex phenotypes and novel developmental mechanisms is presented.

PubMed Disclaimer

Figures

Fig. 1
Fig. 1
A) Mesozoic creatures and landscape. Life reconstruction of the late Jurassic. Note the diverse integuments and appendages present in the dinosaurs, Mesozoic birds and early mammals. Reptiles: Caudipteryx (1), Sinosauropteryx (2), Psittacosaurus (3, a beaked dinosaurs); Sinornithosaurus (4), Pterosaurs (5, dinosaurs glide with skin flaps). Birds: Confuciusornis (6), Changchengornis (7), Liaxiornis (8, a small toothed bird). Mammals: Zhangheotherium (9, an early mammal). For 1 - 5, see table 2 and section 3. From Hou et al., 2003. P. 38. Painted by Anderson Yang. B) Different developmental stages of skin appendage morphogenesis. The principles of skin formation are the same in reptile, birds, and mammals. From dermatomyotomes and other sources, dermal cell precursors migrate in and build presumptive skin and appendages with regional specificities. They share similar hierarchical morphogenesis but acquire variations that lead to different skin appendage phenotypes. Modified from Chuong and Homberger, 2003.
Fig. 2
Fig. 2. Examples of integument appendages from reptiles, birds, and mammals
A) Reptile scales. B) Top, adult chicken foot. H&E stained sections highlighted in the left panel corresponding to the scutate scale and reticulate scale are shown. Bottom, adult chicken body feather. H&E stained sections indicated at the indicated planes corresponding to pennaceous and plumulaceous regions are shown. The dotted lines indicate the ramus. bb, barbule; is, inner surface; os, outer surface; rm, ramus. C) Mammalian skin appendages. Mouse vibrissae hair follicle. H&E staining. Claw morphology: Compared to the long and curved claw in Monodelphis domestica, the claw in the more arboreal species, Marmosa robinsoni, is short. K14-Noggin mutant mice have reduced or no claw compared to wild-type mice (from Plikus et al., 2004 and Hamrick, 2003). Footpads in K14-Noggin and Hoxd13 -/- mutant mice are smaller in size compared to the wild-type mice (from Plikus et al., 2004 and Hamrick, 2003). Volar skin from the digits of Philander opossum and Chironectes minimus (from Hamrick 2003). Dolphin skin. H&E staining.
Fig. 3
Fig. 3. An example of a Mesozoic bird to show the intermediate integument phenotypes
Evolving creatures at this time have overlapping integument phenotypes such as feathered dinosaurs (Fig. 1A, Table 1) or toothed birds. This Longirostravis is the earliest bird we know that has a probing trophism. A) A fossil of the Longirostravis unearthed in the Jehol Biota from the Yixian Formation in northeastern China. B) An artist's conception of the appearance of Longirostravis in life (from Fossil Birds of China, Hou et al., 2003). C) A close up view of the feeding apparatus, showing the presence of teeth within the beak. It is likely the earliest bird to live in a wading habitat. From Hou et al., 2004. D, E) A close up view of the primary and secondary remiges (flight feathers) and their tracings. Note the feather vanes are long and narrow and already start to show left-right asymmetry.
Fig. 4
Fig. 4. An example of molecular morphogenesis of integument appendages
Upper panels show different stages of feather placode, bud, and follicle formation. Major molecular pathways and morphogenetic events are highlighted in the box. Lower panels show cross sections of a feather filament and different stages of branching morphogenesis
Fig. 5
Fig. 5. Morpho-regulation of integument appendages
An example is shown in which multiple ectodermal organs are affected when the BMP pathway is perturbed using K14 driven expression of noggin. A) A prototypic animal showing different kinds of epithelial appendages (from Chuong, 1998). B) Changes of ectodermal organs in K14 noggin mice (from Plikus et al., 2004).
Fig. 6
Fig. 6. Comparison of the origin and evolution of feathers and hairs from scales
Hypothetical models of amniote skin appendage evolution. A) Comparative developmental processes in reptile scale, avian feathers and mammalian hair. B) Two possible models for the evolution of feathers. Experiments show that the barb - rachis model is correct. C) Models for the evolution of hairs.
Fig. 7
Fig. 7. A hypothetical Evo-Devo Space
X coordinate represents new developmental mechanism. Y coordinate represent new phenotypes. They all start from a flat layer of epidermis. Those in the right upper quadrant used more novel developmental mechanisms and are more complex. Arrows indicated possible topological transformation from one form to the other, not necessary indicate the evolutionary process. We are working to reveal the molecular basis of those arrows. The processes are in red, and the names of the forms are in blue. Yellow circle is the cross section of developing feather follicles with brown indicating the position of rachis. For comparison, the stage correspond to those used in Prum, 1999 is indicated in (green). Revised from Chuong et al., 2001.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Alibardi L. Scale morphogenesis during embryonic development in the lizard Anolis lineatopus. J Anat. 1996;188:713–25. - PMC - PubMed
    1. Alibardi L. Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes. J Exp Zool Part B Mol Dev Evol. 2003;298:12–41. - PubMed
    1. Alibardi L, Maderson PFA. Observations on the histochemistry and ultrastructure of the epidermis of the Tuatara, Sphenodon punctatus (Spehnodontida, Lepidosauri, Reptilia): a contribution to an understanding of the lepidosaurian epidermal generation and the evolutionary origin of the squamate shedding complex. J Morphol. 2003;256:111–33. - PubMed
    1. Alibardi L, Sawyer RH. Immunocytochemical analysis of beta keratins in the epidermis of chelonians, lepidosaurians, and archosaurians. J Exp Zool. 2002;293:27–38. - PubMed
    1. Alibardi L, Thompson MB. Fine structure of the developing epidermis in the embryo of the American alligator (Alligator mississippiensis, Crocodilia, Reptilia) J Anat. 2001;198:265–82. - PMC - PubMed