Review
The Early Origin of Feathers

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Highlights

  • Feathers are epidermal appendages comprising mostly corneous β-proteins (formerly β-keratins), and are characteristic of birds today.

  • There are close connections in terms of genomic regulation between numerous regularly arrayed structures in the epidermis, including denticles in sharks, dermal scales in teleost fish, epidermal scales in reptiles, feathers in birds, and hairs in mammals.

  • The discovery that genes specific to the production of feathers evolved at the base of Archosauria rather than the base of Aves or Avialae (birds) is matched by fossil evidence that feathers were widespread among dinosaurs and pterosaurs, the flying reptiles.

  • This suggests that feathers arose first, as simple monofilaments, probably for insulation in the archosaurian ancestors of birds and dinosaurs during the Early Triassic, a time when land vertebrates were speeding up in terms of physiology, with erect gaits and endothermy.

Feathers have long been regarded as the innovation that drove the success of birds. However, feathers have been reported from close dinosaurian relatives of birds, and now from ornithischian dinosaurs and pterosaurs, the cousins of dinosaurs. Incomplete preservation makes these reports controversial. If true, these findings shift the origin of feathers back 80 million years before the origin of birds. Gene regulatory networks show the deep homology of scales, feathers, and hairs. Hair and feathers likely evolved in the Early Triassic ancestors of mammals and birds, at a time when synapsids and archosaurs show independent evidence of higher metabolic rates (erect gait and endothermy), as part of a major resetting of terrestrial ecosystems following the devastating end-Permian mass extinction.

Section snippets

Early Origin of Feathers

It is shocking to realise that feathers originated long before birds because feathers have generally been regarded as the key avian innovation 1., 2., 3., 4.. However, thousands of astonishing fossils from China have shown that many nonavian dinosaurs (see Glossary) also had feathers, including feather types not found in birds today. These discoveries extended the origin of feathers minimally back to ~175 million years ago (Ma), 25 million years (Myr) before the first generally acknowledged

Feathers, Ancient and Modern

A feather comprises a single filament or involves numerous filaments or barbs, which, if connected by a rachis, form a branched structure. The barbs or rachis derive from a hollow calamus, which grows from a circular epidermal wall around a dermal papilla, both being inserted in a follicle. Feathers are made mostly from fibrous corneous β-proteins (abbreviated CBPs; formerly termed β-keratins), the reptile and bird-specific keratin-associated proteins, which not only surround, but substantially

Preservation of Ancient Feathers

The morphology of fossil feathers can be hard to determine because of alteration during the fossilisation process (taphonomy) and the limitations of traditional light microscopy [26]. Furthermore, some authors have queried whether the fossil structures are indeed feathers, favouring an interpretation as dermal collagen fibres [27]. However, this view is not consistent with morphological and taphonomic evidence 1., 28. and is not widely accepted.

New visualisation techniques, such as

Genomic Regulation of Feather Development

A dense pattern of cutaneous appendages covers the body of vertebrates. These include tooth-like scales (denticles or odontodes) in chondrichthyans (sharks and rays) and mineralised dermal scales in actinopterygians (bony fish). Odontodes comprise a base of bone-like tissue and a dentine cone covered by a hypermineralised layer secreted by the epidermis [57]. Alpha-polypeptides of keratins are an evolutionary novelty of vertebrates [58], while CBPs, the toughest natural polymers known [8], are

Feather Evolution

With a rich fossil record, and a robustly supported phylogenetic tree, it is possible to reconstruct the key stages in feather evolution. Most cladistic analyses concur that Pterosauria is nearest major sister group of Dinosauria 78., 79.. The recent [80] rearrangement of the relationships of the three key dinosaurian clades does not affect the analysis of timing of feather origins.

If feathers occur across dinosaurs and pterosaurs, then their origin has to be sought minimally during the Early

Concluding Remarks

Recent work in the developmental biology and palaeontology of feathers has changed our views and opened many new questions (see Outstanding Questions). The new work concurs that these remarkable innovations originated long before the origin of birds, even before the origin of dinosaurs. This does not diminish the importance of feathers as key to the success of birds, but shows that birds did not emerge rapidly from reptiles, but that their set of 30 or more adaptations [78] accumulated stepwise

Outstanding Questions

  • Were feathers present in nonavemetatarsalian archosaurs (i.e., crocodilian ancestors)?

  • Was insulation the initial function of feathers?

  • How can the camouflage and display functions of feathers be tested in fossils?

  • What were the functions of the feather types known only in fossils, and not in modern birds?

  • How did feathers evolve in different groups of pterosaurs, dinosaurs, and birds?

  • Melanin occurs in protofeathers, but when did the diversity of other pigments appear in feathers?

  • When did feathers

Acknowledgements

We received detailed and very helpful advice from Lorenzo Alibardi and the reviewers, including Michael Pittman, and three anonymous colleagues.

Glossary

Archosaur
a member of clade Archosauria, including birds, crocodilians, dinosaurs, and all their ancestors back to the Late Permian.
Arms race
a form of competition where two clades interact directly over a span of time, sometimes as predators and prey, which then evolve adaptations and counter-adaptations against each other.
Autolithification
processes by which bacteria seal and preserve organisms such that their soft tissues are mineralised rapidly
Avemetatarsalians
members of the wider clade that

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