Evolution of brilliant iridescent feather nanostructures

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The brilliant iridescent plumage of birds creates some of the most stunning color displays known in the natural world. Iridescent plumage colors are produced by nanostructures in feathers and have evolved in a wide variety of birds. The building blocks of these structures—melanosomes (melanin-filled organelles)—come in a variety of forms, yet how these different forms contribute to color production across birds remains unclear. Here, we leverage evolutionary analyses, optical simulations and reflectance spectrophotometry to uncover general principles that govern the production of brilliant iridescence. We find that a key feature that unites all melanosome forms in brilliant iridescent structures is thin melanin layers. Birds have achieved this in multiple ways: by decreasing the size of the melanosome directly, by hollowing out the interior, or by flattening the melanosome into a platelet. The evolution of thin melanin layers unlocks color-producing possibilities, more than doubling the range of colors that can be produced with a thick melanin layer and simultaneously increasing brightness. We discuss the implications of these findings for the evolution of iridescent structures in birds and propose two evolutionary paths to brilliant iridescence.

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  1. Evaluation Summary:

    Nordén et al. examine feather iridescent color diversity across bird species. Their findings show how key modifications in feather melanosomes, pivotal nanophotonic structures, underlie the brilliant colors of iridescent feathers, broadening feather color range approximately twofold. In a next step, the authors evaluate the function of feather melanosomes by performing optical modelling of nanostructure diversity, evaluating up to 4500 distinct nanostructure combinations, which are then contrasted with the observed (color) spectral data from 120 plumage regions across 80 (diverse) bird species. This meticulous integration of diverse methods across a comprehensive dataset will not only inform biologists studying structural color biodiversity, but it may also inspire engineers designing nanophotonic systems.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

  2. Reviewer #1 (Public Review):

    Nordén et al. investigated the mechanisms that underlie the brilliant colours of iridescent feathers that more than double the range of colours. They successfully do this first by identifying the three key modifications of melanosomes in brilliant iridescent structures, followed by extensive optical modelling of nanostructures (up to 4500 different combinations) which is validated by spectral data from 120 plumage regions across 80 diverse bird species.

    The conclusions of this paper are well supported and I have only few minor suggestions left for the authors. The strength of this paper is not in the novelty of the hypothesis (the importance of thin layers for iridescence is well known), however, as the researchers point out they are the first to place this in a broader context identifying out some general principles that underlie irididescent colour production. The methodology used is state-of-the art and the dataset used is relatively big. The major methodological weakness, if there is any, would be that the validation dataset is a bit low (80 species) which might explain why some patterns observed in the optical simulations were not recovered in the real feathers. However, I think the authors provide a sound explanation of why simulations and feathers not always agree, so I'm not sure if adding more reflectance measurements is necessary. Additionally, in the introduction the question "Why have bird species with brilliant iridescence evolved not one but four different melanosome types?" is, for me, not entirely solved and is out of the scope of this manuscript and I would have like more functional and mechanism-related questions such as "at what point are melanosomes too thick to make iridescent color?". Regardless, I do believe that this manuscript is a good starting point to solve other evolutionary questions. In addition to providing a census on how iridescent colouration is produced, and what the effects are on colour diversity, it provides an overview of where these different mechanisms are present. In this way, future work can use this dataset to test additional evolutionary and genetic questions currently unsolved.

  3. Reviewer #2 (Public Review):

    In this manuscript, the authors aimed to identify the mechanisms that separate 'brilliant' from 'weakly' iridescent feathers in birds. Specifically, by leveraging theoretical predictions and the diversity of melanosome shapes in birds, the authors were able to conclude that thin melanin layers were the primary mechanism driving the production of 'brilliant' iridescence. FDTD models of bird melanosomes further support their conclusions that thin layers can greatly expand the range of possible colors that can be produced.

    The volume and comprehensiveness of the data in this manuscript will be greatly beneficial to others studying structural color, and there is good alignment between theoretical predictions, morphological observations, and model results. Further, despite some discrepancies between the optical modeling results and the results from spectrophotometry (a common issue in any FDTD modeling comparison) the authors did a thorough job of reconciling those differences with the available data. Finally, the authors do a good job of walking the reader through each set of predictions and comparing those predictions to their results. This adds significant value as a framework for others investigating iridescence across taxa, or researchers exploring specific clades of birds in detail.