Two waves of adipogenesis in developing avian skin and dermal plasticity

How the complex architecture of skin is constructed, balancing both similarity and adaptive diversity, is not well understood. We propose that the developmental assembly of skin components, including skin appendages, dermal muscles, dermal adipose tissues, and vasculature, is interdependent and adaptive, enabling different species to adjust to their respective environments. Using the developing chicken skin model, we recently demonstrated that the intradermal muscle network and vasculature are organized with feather buds as reference points during the process of adaptive tissue patterning. In this study, we investigate the development of adipose tissue in the avian skin and compare them in different avian species (chicken, quail, duck). Avian skin contains two types of adipose tissue: subcutaneous white adipose tissue (SWAT) is skin associate adipose tissue located in subcutaneous layer, while dermal white adipose tissue (DWAT) consists of a layer of adipocytes within the dermis. Using elastin to distinguish dermal and subcutaneous layers, we observed two distinct waves of adipogenesis, shown by Oil Red O staining. The first wave, representing SWAT, begins around chicken embryonic day 14 (E14) from the posterior dorsal region. These adipocyte clusters are aligned with vasculatures. The second wave, representing DWAT, starts around E16, from the body midline where feather buds are more mature and starts to form smooth muscle network. DWAT adipocytes appear around feather follicles and align with the intradermal smooth muscle network, forming a grid pattern. The association between DWAT and dermal muscle was further explored. Some SMA-positive cells show co-expression of early adipocyte markers, suggesting a shared lineage. Lineage tracing using SMA-Cre revealed that some SMA + cells in developing skin can give rise to adipocytes, shown by co-staining with the C/EBPα antibody. To explore differences of adipose tissues in birds living in different environments, we examined aquatic bird duck. In the duck, the first wave of SWAT appears in embryonic development from both scapular and femoral regions, while the second wave of DWAT also starts from the midline, surrounding feather follicles. Both waves are significantly more abundant in ducks, reflecting the adaptation in the duck skin. These findings suggest developmental relationships among tissue components in the skin-such as feathers, fat, vasculature, and dermal smooth muscle-are interconnected and adaptive, setting up the foundation for further investigation on regulatory mechanisms of dermal plasticity.