Feathers with Ocular Architecture: Implications for Functional and Evolutionary Similarities of Visual Signals and Receptors

Studies of visual receptors typically assume that only functionally similar structures are relevant to the evolution of complex eyes. This approach ignores growing evidence that different functional classes of organs often share structural and developmental patterns that pertain to biological sameness (deep homology). However, the potential relevance of non-receptor structures to eye evolution remains largely unexplored. An “ocular” feather color mechanism is described whose structural and optical features resemble those of chambered, image-forming eyes to a remarkable degree. These similarities include a laterally expanded, domed light receiving surface similar to that of an eye, an encapsulated spongy tissue mass whose coherent light scattering properties in the human-visible (destructive) and ultraviolet (constructive) wavelength ranges resemble those of cornea and lens, intervening spaces such as those with humors, and a laminar pigmented shelf whose structure and optics resemble a mirrored tapetum lucidum found behind many retinas. Fourier analysis and optical principles indicate that ocular structures adhere to the same light-handling properties regardless of higher function (receptor or signal). The extent to which chambered eyes and ocular feathers have evolved independently is surprisingly equivocal. On the one hand, broad differences in the location, composition, and development of chambered eyes and ocular feather signals suggest convergent evolution on an ocular organization. However, some level of evolutionary parallelism (generative homology) between chambered eyes and ocular feathers is implicated by similarities in constructional materials, tissue development, and signal transduction cascades. Structural, optical, and developmental similarities also occur between more primitive eyes and the colored dermal papillae responsible for avian skin ornamentation. Functional constraints on light-handling requirements, coupled with developmental constraints in high-stress environments on the body surface, may enhance the similar evolutionary outcomes in the different functional setting. Regardless of the mechanistic details, repeated evolution of eye-like structures in different functional settings reveals a biological potential to produce such organs that is much greater than would be inferred from a survey of receptor structures alone.