bioRxivEvolutionary BiologyPreprint
Modulation of Avian Iridescence via Melanogenesis
Soraia BarbosaiD, Carina Bittner, Roberto ArboreiD, Pedro M. AraújoiD, Paulo PereiraiD, Pedro AndradeiD, Csaba FeketeiD, Rita O. AfonsoiD, Sandra AfonsoiD, Maria Amorim, Cristiana I. MarquesiD, Michaël P. J. NicolaïiD, Joao CaritaiD, Jindřich BrejchaiD, Ricardo Lopes, Joel Alves, Fernando CruziD, Jèssica Gómez‐GarridoiD, Cristina Zamarreño PastoriD, Marta Ortova GutiD, Tyler AliotoiD, Muhammad Akhtar AliiD, Andrea Hilpert, Anita Hech, Erdmann SpieckeriD, , Miguel CarneiroiD
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Abstract
The iridescent colors of birds originate in nanoscale feather structures that interact with light. Although the physical principles governing avian iridescence are well-established, the molecular mechanisms assembling these nanostructures into photonic materials remain unknown. Here, we integrated genomic, cellular, and optical approaches to investigate the molecular basis of iridescent color formation in birds. We leveraged mutations that arose in the domesticated Indian peafowl and natural color variation in wild birds. In peafowl, we identified eight genes underlying gains, losses, and shifts of iridescence, whereas in two wild species, we used single-cell transcriptomics to profile asymmetric feathers in which iridescent and non-iridescent barbules develop on opposite sides of the same feather. We found that all peafowl mutations mapped to melanogenesis genes, showing that variation in this pathway can modify diverse geometric features of feather photonic nanostructures. Mutations altering melanin composition collapsed multilayered photonic systems and yielded non-iridescent tissues, whereas changes in melanosome abundance, elongation, or deposition timing generated multilayer architectures with variable periodicity and color. We further show in peafowl that transitions from non-iridescent to iridescent plumage were associated with single-nucleotide mutations in a melanogenesis gene, suggesting that, in species already capable of forming multilayered nanostructures, iridescence can be gained by relatively small genetic changes. Single-cell transcriptomes from wild species also supported extensive melanocyte-centered regulatory rewiring associated with iridescence, including changes in melanosome maturation, trafficking, and intercellular signaling. Together, these results show that the nanoscale order underlying iridescence is developmentally plastic and highly responsive to the melanogenic environment. Significance StatementBird feathers can produce brilliant, shifting colors, but how these colors form during development has remained poorly understood. By comparing the genomes of color variants of domesticated peafowl and transcriptomes during feather development in wild birds, and combining these with chemical and optical analyses, we show that mutations in genes associated with melanogenesis can profoundly alter the amount, shape, and arrangement of the melanin granules inside feathers that interact with light and produce iridescence. These changes can switch feather appearance between dull and iridescent, or generate entirely new colors by restructuring how those granules are layered at the microscopic scale. Our results reveal a direct and flexible link between pigment production and the physical structures that generate iridescence in birds.
- organism: zebrafish
- assay: scRNA-seq
- research focus: cell type annotation
- research focus: differential expression
- approach: genetic perturbation / CRISPR
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