Feather Gene Expression Elucidates the Developmental Basis of Plumage Iridescence in African Starlings

Abstract

Iridescence is widespread in the living world, occurring in organisms as diverse as bacteria, plants, and animals. Yet, compared to pigment-based forms of coloration, we know surprisingly little about the developmental and molecular bases of the structural colors that give rise to iridescence. Birds display a rich diversity of iridescent structural colors that are produced in feathers by the arrangement of melanin-containing organelles called melanosomes into nanoscale configurations, but how these often unusually shaped melanosomes form, or how they are arranged into highly organized nanostructures, remains largely unknown. Here, we use functional genomics to explore the developmental basis of iridescent plumage using superb starlings (Lamprotornis superbus), which produce both iridescent blue and non-iridescent red feathers. Through morphological and chemical analyses, we confirm that hollow, flattened melanosomes in iridescent feathers are eumelanin-based, whereas melanosomes in non-iridescent feathers are solid and amorphous, suggesting that high pheomelanin content underlies red coloration. Intriguingly, the nanoscale arrangement of melanosomes within the barbules was surprisingly similar between feather types. After creating a new genome assembly, we use transcriptomics to show that non-iridescent feather development is associated with genes related to pigmentation, metabolism, and mitochondrial function, suggesting non-iridescent feathers are more energetically expensive to produce than iridescent feathers. However, iridescent feather development is associated with genes related to structural and cellular organization, suggesting that, while nanostructures themselves may passively assemble, barbules and melanosomes may require active organization to give them their shape. Together, our analyses suggest that iridescent feathers form through a combination of passive self-assembly and active processes.

Evolution of brilliant iridescent feather nanostructures

“…To test our hypotheses, careful characterization of nanostructures in a group with repeated transitions to brilliant iridescence is needed. Such a study could also lay the groundwork for exploring the genetic regulation of iridescent structures, an area of research in its infancy ( Saranathan and Finet, 2021 ; Rubenstein et al, 2021 ; Price-Waldman and Stoddard, 2021 ).…”

Pterin-based pigmentation in animals

“…This debate has been driven in large part by studies in birds [102][103][104], for which melanin is typically linked to a cryptic function (but many examples show melanins contribute to non-cryptic displays, e.g. [105][106][107]), while dietary carotenoids are typically used for bright displays. Pterins can play a major role in informing this debate given they are predominantly used for conspicuous signalling, so should be a prime target to test if the relative importance of resource allocation versus linkage to vital pathways is maintained across major pigment types.…”

Cortex Thickness Is Key for the Colors of Iridescent Starling Feather Barbules With a Single, Organized Melanosome Layer

“…An extensive comparative study on the melanosomes of African starlings demonstrated that the melanin granules of Lamprotornis may be short and thick as well as slender and elongated (Craig and Hartley, 1985). Evolutionary transitions between rodlets and platelets have been recently suggested for starlings (Maia et al, 2013;Rubenstein et al, 2021). Furthermore, the interior of the melanosomes is presumably not fully hollow as TEM studies showed the existence of minor cross-linking elements (Figure 6E).…”