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The Making of a Flight Feather: Bio-architectural Principles and Adaptation

  • Wei Ling Chang
  • , Hao Wu
  • , Yu Kun Chiu
  • , Shuo Wang
  • , Ting Xin Jiang
  • , Zhong Lai Luo
  • , Yen Cheng Lin
  • , Ang Li
  • , Jui Ting Hsu
  • , Heng Li Huang
  • , How Jen Gu
  • , Tse Yu Lin
  • , Shun Min Yang
  • , Tsung Tse Lee
  • , Yung Chi Lai
  • , Mingxing Lei
  • , Ming You Shie
  • , Cheng Te Yao
  • , Yi Wen Chen
  • , J. C. Tsai
  • Shyh Jou Shieh, Yeu Kuang Hwu, Hsu Chen Cheng, Pin Chi Tang, Shih Chieh Hung, Chih Feng Chen, Michael Habib, Randall B. Widelitz, Ping Wu, Wen Tau Juan*, Cheng Ming Chuong
*Corresponding author for this work
  • China Medical University Taichung
  • National Cheng Kung University
  • Academia Sinica - Institute of Physics
  • University of Southern California
  • CAS - South China Institute of Botany
  • National Chung Hsing University
  • University of Texas at Arlington
  • Asia University Taiwan
  • National Taiwan University
  • Council of Agriculture Taiwan
  • Natural History Museum of Los Angeles County

Research output: Contribution to journalArticlepeer-review

Abstract

The evolution of flight in feathered dinosaurs and early birds over millions of years required flight feathers whose architecture features hierarchical branches. While barb-based feather forms were investigated, feather shafts and vanes are understudied. Here, we take a multi-disciplinary approach to study their molecular control and bio-architectural organizations. In rachidial ridges, epidermal progenitors generate cortex and medullary keratinocytes, guided by Bmp and transforming growth factor β (TGF-β) signaling that convert rachides into adaptable bilayer composite beams. In barb ridges, epidermal progenitors generate cylindrical, plate-, or hooklet-shaped barbule cells that form fluffy branches or pennaceous vanes, mediated by asymmetric cell junction and keratin expression. Transcriptome analyses and functional studies show anterior-posterior Wnt2b signaling within the dermal papilla controls barbule cell fates with spatiotemporal collinearity. Quantitative bio-physical analyses of feathers from birds with different flight characteristics and feathers in Burmese amber reveal how multi-dimensional functionality can be achieved and may inspire future composite material designs. Video Abstract: [Figure presented] The design and developmental paradigms of flight feathers are explored using a combination of bio-physical analyses, molecular characterization, and evolutionary comparisons across a broad range of birds with different flight modes, revealing a modular architectural design that can accommodate diverse eco-spaces.

Original languageEnglish
Pages (from-to)1409-1423.e17
JournalCell
Volume179
Issue number6
DOIs
StatePublished - 27 Nov 2019
Externally publishedYes

Keywords

  • amber
  • branching morphogenesis
  • composite biomaterials
  • dermal papilla
  • development
  • evolution
  • feathered dinosaurs
  • keratin
  • morphogenesis
  • stem cells

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