Published May 16, 2024 | Version v1
Journal article Open

Conserved regulatory switches for the transition from natal down to juvenile feather in birds

  • 1. University of Southern California
  • 2. Academia Sinica
  • 3. Shenzhen University Medical School
  • 4. National Center for High-performance Computing
  • 5. University of Michigan
  • 6. National Chung Hsing University
  • 7. University of Chicago

Description

The transition from natal downs for heat conservation to juvenile feathers for simple flight is a remarkable environmental adaptation process in avian evolution. However, the underlying epigenetic mechanism for this primary feather transition is mostly unknown. Here we conducted time-ordered gene co-expression network construction, epigenetic analysis, and functional perturbations in developing feather follicles to elucidate four downy-juvenile feather transition events. We report that extracellular matrix reorganization leads to peripheral pulp formation, which mediates epithelial-mesenchymal interactions for branching morphogenesis. α-SMA (ACTA2) compartmentalizes dermal papilla stem cells for feather renewal cycling. LEF1 works as a key hub of Wnt signaling to build rachis and converts radial downy to bilateral symmetry. Novel usage of scale keratins strengthens feather sheath with SOX14 as the epigenetic regulator. We show that this primary feather transition is largely conserved in chicken (precocial) and zebra finch (altricial) and discuss the possibility that this evolutionary adaptation process started in feathered dinosaurs.

Data availability

The authors declare that all data supporting the findings of this study are available within the article and its Supplementary Information files, or are available from the authors upon request. The source data for Figs. 2, 4, and 5, Methods, Supplementary Figs. 3–5, and Table 1 are provided as a Source Data file. High throughput sequencing data have been deposited in the NCBI Sequence Read Archive (SRA) under BioProject ID: PRJNA1084783. Source data are provided with this paper.

The codes used for TO-GCN analyses are available at https://github.com/petitmingchang/TO-GCN https://github.com/petitmingchang/TO-GCN. The codes used for ATAC peak visualization and other analysis are available at https://github.com/r93b42016/feather_transition

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Additional details

Identifiers

DOI
10.1038/s41467-024-48303-3
Other
oai:uchicago.tind.io:11905

Funding

National Science and Technology Council, Taiwan
NSTC 112-2311-B-045-3
National Institutes of Health
RO1 AR 047364
National Institutes of Health
R37 AR 060306
Unknown funder
China Medical University (in Taiwan)—University of Southern California collaborative grant
Ministry of Education in Taiwan
Higher Education Sprout Project
Dragon Gate Program
112-2926-I-006-507-G
University of Southern California
CIRM COMPASS Scholars Program

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Ecology and Evolution