A meta-analysis of butterfly structural colors: their color range, distribution, and biological production
Data files
Sep 22, 2023 version files 123.40 KB
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Database_butterfly_structural_colors.txt
113.28 KB
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README.md
10.12 KB
Abstract
Butterfly scales are among the richest natural sources of optical nanostructures, which produce structural color and iridescence. Several recurring nanostructure types have been described, such as ridge multilayers, gyroids, and lower lamina thin films. While the optical mechanisms of these nanostructure classes are known, their phylogenetic distributions and functional ranges have not been described in detail. In this Review, we examine a century of research on the biological production of structural colors, including their evolution, development, and genetic regulation. We also create a database of more than 300 optical nanostructures in butterflies and conduct a meta-analysis of the color range, abundance, and phylogenetic distribution of each nanostructure class. Butterfly structural colors are ubiquitous in short wavelengths but extremely rare in long wavelengths, especially red. In particular, blue wavelengths (around 450 nm) occur in more clades and are produced by more kinds of nanostructures than other hues. Nanostructure categories differ in prevalence, phylogenetic distribution, color range, and brightness. For example, lamina thin films are the least bright; perforated lumen multilayers occur most often but are almost entirely restricted to the family Lycaenidae; and 3D photonic crystals, including gyroids, have the narrowest wavelength range (from about 450 to 550 nm). We discuss the implications of these patterns in terms of nanostructure evolution, physical constraint, and relationships to pigmentary color. Finally, we highlight opportunities for future research, such as analyses of subadult and Hesperid structural colors and the identification of genes that directly build the nanostructures, with relevance for biomimetic engineering.
README
This README file was generated on 2023-09-22 by Rachel C. Thayer.
GENERAL INFORMATION
- Title of dataset: A meta-analysis of butterfly structural colors: their color range, distribution, and biological production
- Author for correspondence: Name: Rachel C. Thayer Institution: University of California, Davis Email: thayerr@berkeley.edu
- Data was derived from the following sources:
- 187 previously published studies from the years 1940-2023. See the dataset variable entitled 'References' for details.
- Information about funding that supported the data curation: NSF-DEB-1601815.
SHARING/ACCESS INFORMATION
- Licenses/restrictions placed on the data: CC0 1.0 Universal (CC0 1.0) Public Domain
- Links to other publicly accessible locations of the data: None
- Was data derived from another source? YES A. If yes, list source(s): See dataset variable entitled 'References'
- Recommended citation for this dataset: Thayer, R.C. and Patel, N.H. (2023). A meta-analysis of butterfly structural colors: their color range, distribution, and biological production. Journal of Experimental Biology.
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DATA-SPECIFIC INFORMATION FOR: Database_butterfly_structural_colors.txt
- Number of variables: 20
- Number of cases/rows: 420
- Field delimiting character: This is a tab-delimited file
- Description: This database organizes previously published data on optical nanostructures that produce structural color in butterflies. It can be used to identify structures that are good candidates for further characterization, to explore the evolutionary history and realized functional limits of several different types of optical structure, and to identify butterfly taxa whose optical nanostructures have been understudied to date, among other uses. Each row describes one putative optical nanostructure, occuring in a butterfly species, as reported by a broad literature survey.
- Variable List:
- Species: Species from which the optical nanostructure was isolated. A species may occur in more than one row within the dataset if more than one optical nanostructure has been characterized from the species, such as scales sampled from differently colored wing regions, or sexually dimorphic scales from each sex.
- Family: Family-level taxonomic classification to which the specimen belongs
- Subfamily: Subfamily-level taxonomic classification to which the specimen belongs. Missing data means the specimen was not precisely identified.
- Structure_type: This column gives the unifed term used to categorize the structure in figures 2-4 in the corresponding publication. "lumen_PF" = perforated multilayer in the lumen; "lumen_3D" = 3D photonic crystal in the lumen; "lamina" = lower lamina thin film reflector; "crossrib" includes crossrib bilayers with and without air columns and one instance of a crossrib multilayer; "lumen_smoothmulti" = continuous multilayer in the lumen; "ridge" = ridge multilayer; for "other" see the structure_notes variable or the accompanying publication for details. Scales with more than one optical nanostructure have two values separated by a comma in this field, see publication also for further explanations. Missing data means that there is insufficient data to confidently assign the structure to one of the aforementioned categories.
- structure_notes: Additional commentary on the structure type and its optical mechanism. The commentary may include justification for the assignment in the structure_type variable, further details on the structure type especially if it belongs to the "other", or "crossrib" category, or a brief description of putative optical structures turned up by the literature review that could not be categorized. This field contains free-form text and may include space and punctuation characters.
- color_notes: Notes about the color of the structure. May give more detail than the variable 'Color_qualitative'. This field includes free-form text and may include space or punctuation characters.
- Color_qualitative: Unified terms describing the qualitative color of the structure, if a qualitative description is the best color data available. Possible values are [pearl, white, blue, black, silver, pearl, gold, grey, magenta, orange, pink, green, blue-green, UV, violet, yellow-green, bronze]. This field is missing if a quantitative color value is available in the variable max_WL, or if there is no color information available at all. This variable is used in Fig. 2 in the corresponding publication.
- max_WL: The wavelength of maximal reflection, measured in nanometers, i.e. the "hue". See Methods for details on how this was determined when multiple spectroscopy measurements were found in the literature review.
- brightness: The percent reflectance of the maximally reflected wavelength given in variable max_ML, i.e. the brightness.
- angle_illum: The angle of illumination that is associated with the reflectance spectral data, measured in degrees. 'Normal' = 90 degrees. Missing data means this information was not reported in the original data source. The field may contain a brief description if it could not be accurately summarized as a single number, for example "approximately normal but with a range of 15 degrees." If reported methods only stated that a microspectrophotometer was used, I assumed a 90 degree illumination angle.
- angle_obs: The angle of observation that is associated with the reflectance spectral data, measured in degrees. 'Normal' = 90 degrees. An "integrated" value in this field means reflected light was collected by an integrating sphere. An empty field means this information was not reported in the original data source. If reported methods only stated that a microspectrophotometer was used, I assumed a 90 degree observation angle.
- reflectance_notes: Reflectance notes summarizes in more detail the published reflectance spectra. Where applicable, information in this field includes the maximum wavelength and the brightness for each available measurement when the structure has been measured by multiple studies, from multiple specimens, or with alternate methods. For example, if a study by Wilts et al. measured a maximal reflectance of 15% at 450 nm, this field would include "Wilts: 450x15". Where methodology was adequately described by the original study, these notes also include some methodology details, particularly whether spectra were taken from an intact wing region versus from a single isolated scale, and whether an integrating sphere ('int sphere') or a microspectrophotometer ('microspec') was used.
- evidence: A semi-colon delimited list of the types of data available to characterize the structure, such as electron micrographs (SEM or TEM), reflectance measurements, modeling work to explore or confirm its optical mechanism, scatterometry, absorption measurements, light polarization measurements, or x-ray scattering (SAXS). Empty field means none of these data types were found.
- in_cover_scale: Reports whether the nanosturcture occurs in cover scales as 'Y' = yes or 'N' = no. Empty field means the source data did not specify which scale type contained the nanostructure. There is one cell with a value "maybe weakly", meaning the nanostructure may occur in cover scales in a less developed state.
- in_ground_scale: Reports whether the nanostructure occurs in ground scales. Possible values are 'Y' = yes, 'N' = no, or a brief statement in cases where the answer involves more nuance. Empty field means the source data did not specify whether the structure occurred in ground scales.
- co-occurring_pigment: Reports whether there is a co-occurring pigment in the scale, and if so, identifies what kind of pigment it is--by name, by color, by its wavelength of peak absorption, or otherwise. Possible values include but are not limited to [yes, no, probably not, maybe]. An empty field means the presence or absence of pigment has not been determined. This field can include punctuation and space characters.
- Variation_documented: Reports whether there is any documentation of variation in either the structure's morphology or its color. This could include data from more than one scale, more than one individual, or more formal comparisons between populations, sexes, etc. The field may simply give 'Y' for yes, or it may briefly give details on the sample size. 'N' or empty field mean the sample size was n=1, i.e. no documentation of variation.
- Specimen_metadata: Reports whether metadata on the butterfly specimens was provided, such as GPS locality data, collection region and altitude, collection date and time, and habitat description. The format is a list of values separated by ';'. An empty field means specimen metadata was not reported.
- References: A list of studies that provide the original source data, separated by semi-colons. The literature list may also include studies that provide additional context, such as experiments testing the ecological function of the structure. Reference format is as follows: Surname of the first author, year, abbreviated journal title, e.g. 'Stavenga 2011 J Exp Bio'. If the reference source is not a journal article, it is labeled "undergraduate thesis", "MS thesis" = master's thesis, (dissertation)= doctoral dissertation, or (book chapter).
- other_notes: Other notes. For species that occur in more than one row, i.e. species with multiple structures in different wing regions, this column clarifies which structure / wing region / sex is the focus of the row. This field may also mention any other point of interest or clarification regarding the structure. This field may include whitespace and punctuation characters.
- Missing data codes: NA
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CODE/SOFTWARE
- The R code used to analyze this dataset for the corresponding publication is provided at https://doi.org/10.5281/zenodo.8215997. It was run in R version 3.2.2.
Methods
Several intersecting approaches were used to search for articles, book chapters, and theses reporting nanostructures that produce structural colors in butterflies. First, Google Scholar searches were run with combinations of these keywords: structural color, butterfly, Lepidoptera, iridescence, scale, and Ghiradella. Database searches brought up tens of thousands of hits, many of which were not pertinent, so we used high-quality results to find cited and citing references and noted every species that was mentioned in connection with structural color, iridescence, or derived scale morphology. Finally, a database search was run on each species name that had been mentioned in any prior included reference. When a search on species name returned many results, it was searched again in combination with the keywords. If the search on species name returned no relevant results, we tried searches with only the genus name and checked for alternate nomenclature. We continued snowballing references and running database searches on species until we could no longer find any new taxa mentioned in connection with structural color. Criteria for inclusion were that the article must include either (1) reflectance measurements or (2) electron microscope images of non-transparent (i.e. colored) optical nanostructures in a butterfly. We also included studies which provided additional characterizations (e.g. absorption measurements, mathematical modeling, scatterometry) for structures that had been included on the basis of (1) or (2).
This literature review strategy yielded 187 included references which described 421 potential structures from 378 species, all of which are included in this dataset. Before further analysis, we secondarily excluded entries that were presented as non-photonic comparisons to structurally colored specimens. Only seven reported structures occurred outside adult wing scales, which were all multilayer broadband reflectors in the pupal cuticle (Neville, 1977; Steinbrecht, 1985; Steinbrecht et al., 1985). We therefore narrowed our focus to structures located in scales or bristles on the adult, which can be homologized and directly compared in subsequent analyses. After filtering, there was pairwise complete data on both color and morphology for 314 optical nanostructures from 287 species. Some species had multiple structural colors on different body parts (e.g. blue dorsal and green ventral wings in Cyanophrys remus and Albulina metallica; Biró et al., 2007).
To compare color between structures, we recorded the peak reflected wavelength (i.e. hue) and the percent reflectance at that wavelength (i.e. brightness) for each structural color. Due to iridescence, quantification of structural color is extremely sensitive to the measurement protocol, specifically illumination and detection angles, light source, reference sample, and spot size (Meadows et al., 2011). Spectroscopy methodologies were variable among the included studies making comparisons imperfect; nevertheless, the data are useful to show broad trends. When multiple spectra were available, we used the following rules for consistency. When reflectance was reported from more than one angle, the peak wavelength at the maximally reflective angle was used. If comparable reflectance data was reported from more than one study or from replicated specimens, we took their average. When reflectance data was found for both an isolated scale and the intact wing, both values were noted, but the intact wing reflectance was preferentially used in comparative analyses for consistency, because single-scale reflectance measures were uncommon. In cases where structures produced two reflectance peaks – as in Chrysozephyrus species with both a UV and a green peak (Imafuku, Hirose and Takeuchi, 2002) – the brighter peak was used in graphical summaries, but both were listed in the spreadsheet. Peak wavelengths were typically estimated by eye from graphs, which limited precision to a 5–10 nm window around the measured peak. This precision limit is similar to the magnitude of inter-individual variation (Imafuku, Gotoh and Takeuchi, 2002; Bálint et al., 2008). We also recorded percent reflectance at the maximally reflective wavelength (i.e. spectral intensity or ‘brightness’). When no reflectance spectra were available but a color image or a qualitative color descriptor (e.g. ‘blue’, ‘UV’) was given, the qualitative descriptor was recorded. Broadband reflectors have a similar reflectance intensity across many wavelengths, so the maximally reflecting wavelength is not a good summary of the reflector’s properties and may not be identifiable from a visual inspection of a graph. Therefore, for broadband reflectors, we only recorded a qualitative descriptor, such as ‘white’, ‘silver’, or ‘gold’. Additionally, some reddish lamina thin films that reflected in both violet and red, without a peak wavelength in either region, were handled as qualitatively ‘magenta’. Note that many reflectance spectra were likely influenced by co-occurring pigments as well as the nanostructures.
To compare scale morphological modifications, we noted which kind of optical nanostructure was present. Generally, we followed the author’s conclusion as to which scale component caused the optical properties. If the author’s description was brief but a micrograph was provided, we assigned the structure to the same category as the well-studied examples that it most resembled. In a few cases when the proposed mechanism seemed questionable, we noted the explanation in the spreadsheet but dropped that structure from comparative analysis (for example, the proposed nanostructure was not present in the provided micrograph, or the mechanism was disputed across studies). Filled-in windows and crossrib air columns likely involve modifications to both the crossribs and microribs, and reflectance in these scales also requires the lower lamina; for simplicity, we have summarized them as crossrib bilayer structures.
Data was processed using R.