Historical contingency influences the diversity of feather nanostructures in cuckoos

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Abstract
Structural coloration is widespread in animals, yet we know relatively little about its evolution and development. While previous studies have explored adaptive functions of structural color, a key gap is our lack of understanding of how historical contingency (path-dependency of biological processes) influences the loss and gain of this complex trait. We shed light on this question by describing feather nanostructures responsible for plumage colors in the cuckoos (family Cuculidae), a group with widespread occurrence of shiny, metallic plumage (metallic luster). The melanosomes found in feathers with metallic luster have specialized shapes: hollow rods, thin solid rods, hollow platelets, or solid platelets. In contrast, it is generally assumed that drably colored feathers possess thick, rod-shaped melanosomes. However, we uncover that this assumption is unfounded in cuckoos. We describe metallic luster in the plumages of 126 cuckoo species and map its phylogenetic distribution. This reveals that metallic luster is widespread in cuckoos but has likely been lost several times. We then use transmission electron microscopy to describe the feather nanostructures of 21 cuckoo species. Surprisingly, the drab feathers of many cuckoo species contain melanosomes with specialized shapes. We propose that historical contingency greatly influences nanostructure diversity in cuckoos. Specialized melanosome shapes can be retained in the plumages of drab species, potentially making it easier for metallic luster to evolve again in the future. This discovery supports the idea that historical contingency plays a key role in shaping the evolution of plumage color diversity.

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