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Evolution of Feathers

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Evolution of Feathers Good sex for ferns is all about signal timing p. 423 Any hope for ocean INSIGHTS wildlife? p. 420 PERSPECTIVES EVOLUTION Beyond the rainbow Dinosaur color vision may have been key to the evolution of bird feathers By Marie-Claire Koschowitz,1,2 Christian Fischer,2 and Martin Sander1,3 nce believed to be a diagnostic feature of birds, feathers are now known to have evolved in dinosaurs well before the first birds. In birds, feathers serve several functions: Down feathers insulate the body, Owhereas planar or pennaceous feathers are necessary for flight, communication, cam- ouflage, and brooding (see the first figure). What was their original function in non- avian dinosaurs? Based on a specimen of Archaeopteryx that preserves a spectacular plumage of pennaceous feathers, Foth et al. (1) recently hypothesized that pennaceous feathers did not evolve for flight but for display. Together with insights into body size evolution in dinosaurs along the line to birds (2) and the discovery of protofeathers in early dinosaurs ( 3), these results contrib- ute to an emerging understanding of why pennaceous feathers may have been supe- rior to filamentous protofeathers. Protofeathers presumably evolved in early dinosaurs (see the second figure) (4). Vulturine guineafowl Their main function must have been to in- (Acryllium vulturinum) plumage. sulate, because an increase in growth rate Structural colors like blue was facilitated by a faster metabolism early and violet are displayed in concert with intricate, high-resolution 1Division of Paleontology, Steinmann Institute for Geology, ornamentation. The close-up Mineralogy and Paleontology, University of Bonn, Nussallee 8, shows a specimen in the collection 53115 Bonn, Germany. 2Institute for Zoology and Anthropology, Department of Morphology, Systematics and Evolutionary of the Museum Alexander Koenig. Biology with Zoological Museum, Georg-August-Universität The full-size bird is from Göttingen, Berliner Strasse 28, 37073 Goettingen, Germany. the Zoological Museum of the 3Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA. E-mail: University of Göttingen. [email protected] (CLOSE-UP) OLESCHINSKI AND GEORG FOWL) (GUINEA FISCHER CHRISTIAN CREDITS: PHOTO 416 24 OCTOBER 2014 • VOL 346 ISSUE 6208 sciencemag.org SCIENCE Published by AAAS in dinosaur evolution (5). A faster metabo- lism necessitates body insulation because Pygostylia Avialae without an insulated skin, metabolic en- ergy would be lost as heat instead of being Archaeopteryx available for growth. This is particularly Planar feathers exapted for fight true for small- to medium-sized animals such as early dinosaurs and their juveniles Man Dromaeosauridae because of their poor ratio of body volume ira to body surface. A recent study (2) suggests ptora that body size decreased much faster in the bird stem lineage than in other dino- Oviraptorosauria saurs. For fast-growing, presumably warm- Planar feathers blooded animals (5), such miniaturization Structural color signaling Coelurosauria would only have been possible with suffi- Compsognathidae cient body insulation. Small body size However, protofeathers came at a price: Protofeathers in adult inhibit the loss of structural color signaling ca- structural color signaling pabilities. Structural color signaling is Tyrannosauridae limited in a body cover of flexible hairlike Therop structures such as the filamentous feathers of some birds. The display of structural col- oda ors (including iridescence, vivid blues and Large body size Allosauroidea greens, and ultraviolet reflection) requires Adult scaly Structural color signaling the precise arrangement of light-scattering Dinosauria elements at nanometer scales (6–8). In modern bird feathers, these elements con- Sauropodomorpha sist of keratin, air, and melanosome-based nanostructures ( 7), producing iridescence and saturated color displays that are cen- Ornithischia tral to communication and sexual selection Fast growth (see the first figure) (9). Protofeathers Like every signaling system, structural color signaling involves a receiver: the eye Crocodylia of the (nonhuman) beholder. This raises the question of the visual capabilities of di- nosaurs. Differentiated color vision, much Dia Testudines superior to that of humans and other psi mammals ( 10), is known from virtually da all extant reptiles (see the second figure) ? and in many taxa includes ultraviolet vi- Squamata sion. Phylogenetic inference suggests that dinosaurs were endowed with the highly differentiated color vision of birds (11, 12), Rhynchocephalia termed “tetrachromacy” (the ability to dis- criminate hues ranging from ultraviolet to Tetrachromacy turquoise via a fourth, short-wavelength receptive cone cell; the other three cone Tetrachromacy Planar feathers Filaments/fbers cell types are sensitive to blue, green, and red). Tetrachromacy is a basal characteris- Color vision and feather evolution. Extant lizards, tuatara (Rhynchocephalia), turtles, crocodiles, and birds possess four tic of land vertebrates and widely found in cone cell types (tetrachromacy), enabling highly differentiated color vision that presumably was also present in dinosaurs. other vertebrates and invertebrates (6, 10). Protofeathers probably evolved in early dinosaurs for insulation and preceded planar feathers in coelurosaurians. Planar In addition to protofeathers, several non- feathers, in turn, preceded flight or gliding. Miniaturization along the bird stem line led to a trade-off between color display avian maniraptoran dinosaurs indepen- and insulation, which could have been solved by the evolution of planar feathers serving both functions. dently evolved pennaceous feathers that clearly did not serve in flight (13, 14). Pen- Here, coloration depends on the absence or It appears that in advanced manirap- naceous feathers may have been the solution presence of pigments ranging from reddish toran dinosaurs, this trade-off was solved to the evolutionary trade-off faced by these brown to black. Lacking a coherent surface, through the evolution of a new type of dinosaurs between insulation by protofeath- fur did not allow directed light scattering and skin outgrowth that served insulation and ers (4), increased metabolic rate (5), and min- severely impaired structural color display. display needs at the same time: the pla- iaturization ( 2) on the one hand, and the loss Nocturnal activity patterns and body size nar feather. Planar feathers would have of structural color signaling caused by pro- reduction once again mandated body insula- covered up and partially replaced the fila- tofeathers on the other. Instructive parallels tion, but sophisticated color perception and mentous protofeathers, thus leading to the can be found in early mammalian evolution, signaling lost their importance at night and evolution of contour feathers (the smooth when fur starts to appear in the fossil record. differentiated color vision was lost ( 15). feathers that form the outer covering of SCIENCE sciencemag.org 24 OCTOBER 2014 • VOL 346 ISSUE 6208 417 Published by AAAS INSIGHTS | PERSPECTIVES the plumage), as preserved in the Archaeo- DNA REPLICATION pteryx specimen studied in ( 1). Planar feathers consist of a network of multiple interlocking branches of two or- Terminating the replisome ders (barbs and barbules) that are arranged into two sheetlike vanes horizontally pro- Multiple proteins modify and dismantle a key enzyme truding from a central shaft. Because both the precise arrangement of light scattering after DNA replication terminates elements and the optimal exposition to light are mandatory for structural colors By Stephen P. Bell each Mcm2-7 hexamer, forming the active and iridescence, flattened branching fila- replicative helicase, the Cdc45–Mcm2-7– ments offer several benefits. They provide n a eukaryotic cell, DNA replication GINS (CMG) complex ( 7). DNA unwind- more surface area, maximizing structural begins with the unwinding of double- ing at the origin results in the active CMG color signaling at a macroscopic level. Also, stranded DNA at an origin, followed complex encircling the single-stranded sheetlike surfaces provide optimal physi- by the synthesis of complementary “leading-strand” DNA template. The CMG cal conditions for iridescence and satu- strands that grow bidirectionally along complex forms the foundation upon which rated color production. Finally, a “zip-lock” the original DNA strands (forming a the DNA polymerases and other replisome mechanism created by barbules generates a Ireplication fork) from the origin. This syn- proteins assemble. The resulting repli- canvas for detailed ornamentation (see the thesis is carried out by a complex structure some replicates the associated DNA until first figure), a substantial advantage over called a replisome, the heart of which is a it encounters another replisome and ter- less coherently ordered furlike filaments. A ring-shaped DNA helicase that unwinds minates replication. Although the proteins case in point are birds with furlike plum- the DNA. Two key events occur when rep- and events involved in eukaryotic helicase ages, such as ostriches, cassowaries, and lication forks arising from two different loading and activation have been inten- kiwis, that have reduced feather complex- origins converge. The DNA associated with sively studied, how the replisome is disas- ity and only display drab feather colors each fork first must be fully replicated and sembled upon replication termination
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