4.4 Article Proceedings Paper

Morphogenesis of Iridescent Feathers in Anna's Hummingbird Calypte anna

Journal

INTEGRATIVE AND COMPARATIVE BIOLOGY
Volume 61, Issue 4, Pages 1502-1510

Publisher

OXFORD UNIV PRESS INC
DOI: 10.1093/icb/icab123

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Funding

  1. MURI through the Air Force Office of Scientific Research [FA9550-18-0477]
  2. FWO [G007117N]
  3. HFSP [RGP 0047]

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This study investigates the formation and organization of melanosomes in hummingbird feathers, revealing that they mostly occur through passive self-assembly processes. Melanosomes contain air bubbles or vesicles when formed in pigment-producing cells and drastically expand in size when transferred to neighboring cells. The enlargement is driven by physical constraints and the positioning of the melanosomes within the feather structure.
Color is a phenotypic trait of utmost importance, particularly in birds, which are known for their diverse color signals and color-producing mechanisms including pigment-based colors, light scattering from nanostructured feather tissues and combinations thereof. Bright iridescent plumage colors of hummingbirds are caused by light scattering by an organized array of flattened, pigment organelles, containing air-filled vesicles, called melanosomes. These hollow platelets are organized in multilayer arrays that contain numerous sharp air/melanin refractive index interfaces, producing brilliant iridescent colors. Despite their ecological significance and potential for inspiration of new optical materials, how platelets form and spatially arrange in nanostructures in growing feathers remains unknown. Here, we tested the hypothesis that melanosome formation and organization occurs mostly through passive self-assembly processes by assembling a developmental time series of growing hummingbird feathers using optical and electron microscopy. We show that hummingbird platelets contain air bubbles or vesicles upon their formation in pigment-producing cells, melanocytes. When melanosomes are transferred to neighboring keratinocytes (the cells shaping barbule structure) they drastically expand in size; and variation in this enlargement appears to be driven by physical constraints caused by the placement of the melanosomes within the barbule plate and their proximity to other melanosomes. As the barbule elongates and narrows, polymerizing feather corneous beta-protein orients melanosomes unilaterally, forcing them into a stacked configuration. These results reveal potentially novel forces driving the self-assembly of the nanostructures producing some of the brightest colors in nature.

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