Feather microstructures can remarkably change the appearance of red plumage without any corresponding changes in either pigment concentration or molecule types
Adult male Brazilian tanager (Ramphocelus bresilius) is a member of a sexually dimorphic genus of ... [+]
Many birds have brilliant plumage colors, but why? There are several non-exclusive hypotheses may explain the reason(s) that birds invest so much energy into obtaining colorful pigments and creating ornamental plumages:
- coloration may help species identify each other, so they can avoid producing hybrids, which are often sterile, thereby preventing a waste of time and energy (ref).
- beautiful ornaments may reflect arbitrary aesthetic preferences in the choosing sex (usually the female) (ref), and may either be maintained through a runaway evolutionary process (ref), or may occur as a side effect of selection on another trait such as foraging, which is known as “sensory bias” (ref)
- color may indicate individual quality (“honest signaling hypothesis”) through physiological linkage, resource trade-offs, or direct/indirect costs (ref, ref, ref & ref)
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Of these three hypotheses, the honest signaling hypothesis has received the most attention because because carotenoids that create colors ranging in hue from yellow to orange to red are thought to be honest because they are rare, are costly, require a metabolic trade-off, or are an index of proper metabolic function (ref) in vertebrates. For these reasons, carotenoid-pigmented plumages are viewed as a “textbook example of an honest signal” because this signal appears to be extremely difficult to replicate outside of its natural context.
We do know, for example, that a variety of carotenoids play an array of important roles in proper immune function. But a recent study of red-factor canaries with a mutation that knocks out their tissue carotenoids found no difference in their immune system function (ref), which makes the honest signal hypothesis open to further questions.
Previous studies have also found that plumage nano- and microstructures can dramatically alter the appearance of carotenoid colors, which raises the question: Do microstructures that enhance carotenoid coloration add another level of complexity to the honest signal hypothesis? In short, have brilliantly colorful male birds evolved a way to cheat?
Do birds with carotenoid-pigmented plumage rely on microstructures to cheat?
To better understand the physical basis of colorful plumages as well as the evolutionary selective pressures that favor colorful signals, Dakota McCoy, a graduate student at Harvard University who studies biomaterials and how evolutionary arms races and conflicts of interest are affected by them, examined the carotenoid-based plumages of one particularly colorful genus of tanager, Ramphocelus, that lives in the tropics of South America (Figure 1).
F I G U R E 1. Male Ramphocelus tanagers (top row) have more striking carotenoid-based coloration ... [+]
There are nine species of tanagers in the genus Ramphocelus. All of them are social, sexually dichromatic (i. e.; males and females are distinctly color-coded) and have carotenoid-pigmented plumages. Males have strikingly patterned plumage with strongly contrasting colors — black with red, orange or yellow — whilst the females are either a less intensely colored version of the males, or are brownish or greyish with dull red, orange or yellowish patches.
Ms McCoy and her collaborators examinedtanager specimens housed in the Ornithology Collection at the Harvard Museum of Comparative Zoology. She selected 20 male and female specimens, one from each species in the genus Ramphocelus, for this study.
To document the physical basis of color in both male and female Ramphocelus tanagers, Ms McCoy extracted the carotenoid pigments from feathers, measured their concentrations and identified which carotenoid molecules were present. Surprisingly, she found no differences in either the concentrations nor the types of carotenoid pigment molecules in feathers of males and females of the same species despite males having significantly more saturated color patches (Figure 3).
F I G U R E 3: Males and females (within a species) have significantly correlated carotenoid ... [+]
Despite having similar amounts and types of carotenoid molecules in their feathers, male and female Ramphocelus tanagers have dramatically different appearances. Could this visible difference in plumage color between the sexes be created by feather microstructures?
Microstructures intensify plumage colors in males but not in females
Ms McCoy then examined the microstructures of male and female Ramphocelus tanager feathers. She found that female feathers have microscopic structures that look the same as a typical feather macrostructure, where simple cylindrical barbules extend out from the central cylindrical barb, all aligned in a single plane (Figure 4A).
In contrast, male Ramphocelus tanager feathers have a variety of elaborate microstructures that enhance color appearance (Figure 4B,C,D,E,F), including widely expanded barbs that enhance color saturation (for the same amount of pigment), oblong barbs, strap-shaped barbules (instead of cylindrical barbules), and angled barbules that projected out from the plane of the feather, making the feather appear ‘fuzzy’, rather like a tiny toilet brush. This ‘fuzzy’ morphology reduces total light reflectance to generate dark velvety red feathers (Figure 4E), and is very similar to what Ms McCoy had discovered previously in ‘super black’ feathers (more here), which acts as an optical illusion to enhance nearby color.
F I G U R E 4: Males, but not females, have diverse and elaborate feather microstructure. A. Female ... [+]
But surely, the bright red feather patches and the dark red feather patches could not possibly contain the same carotenoid molecules in the same concentrations?
Microstructure, not carotenoids, differs between bright and dark red patches
To answer this question, Ms McCoy assessed the relative contributions from feather microstructures and from feather pigments and compared the bright shiny red patches to the dark velvety red patches in two species, R. melanogaster and R. dimidiatus (Figure 6).
F I G U R E 6: Microstructure, not carotenoids, differs between bright and dark red patches within a ... [+]
For each bird, feathers from the bright shiny red patches and the dark velvety red patches had very similar concentrations of carotenoid pigments. However, SEM photographs revealed large differences in feather microstructures between the shiny and the velvety patches (Figure 6B,C,E,F). Ms McCoy found that expanded feather barbs (Figure 4E) were associated with bright shiny red color whilst vertically-angled dihedral, or ‘fuzzy’, barbules (Figure 4E) were associated with dark velvety red color. This ‘fuzzy’ barbule shape that is only found in males reflects less light, thus creating a richer, more saturated color, even though females and males have the same types and concentrations of pigments (Figure 3).
Is red plumage an honest signal of condition or not?
This study casts doubt on the idea that carotenoids are costly signals by showing that males and females of the same species have the same amount and types of carotenoid pigment molecules in their feathers. It also brings a new focus onto the idea of whether carotenoids — in Ramphocelus tanagers at least — can be considered “honest” signals because the appearance of these pigments is significantly altered by male-specific feather microstructures.
But are they cheating?
“I think males are ‘stretching the truth’ using structures to look even better for the same amount of pigment”, Ms McCoy explained in email.
“I do not mean to say these signals convey NO true information about male quality”, Ms McCoy added in email. “Many selective forces interact to generate beautiful bird colors: avoiding predation, appealing to potential mates, and — to an extent — honestly signaling your quality.”
The appearance of carotenoid-pigment based coloration as an honest signal of male quality is partially exaggerated by feather microstructures (in this case, microstructures that enhance light-pigment interactions), and these feather microstructures themselves are not necessarily linked to quality. This suggests that feather microstructures arose as part of the evolutionary arms race between female preference and male appearance.
“Males are incentivized to look as good as they can”, Ms McCoy added in email. “When a measure becomes a target, it ceases to be a good measure.”
Source:
Dakota E. McCoy, Allison J. Shultz, Charles Vidoudez, Emma van der Heide, Sunia A.Trauger, and David Haig (2020). Microstructures amplify carotenoid plumage signals in colorful tanagers, bioRxiv preprint | doi:10.1101/799783
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