Hummingbird iridescence: an unsuspected structural diversity influences colouration at multiple scales

Abstract

10Iridescent colours are colours that change depending on the angle of illumination or observation. They are 11 produced when light is reflected by multilayer structures or diffracted by gratings. While this phenomenon is well 12 understood for simple optical systems, it remains unclear how complex biological structures interact with light 13 to produce iridescence. There are very few comparative studies at interspecific level (often focusing on a single 14 colour patch for each species), resulting in an underestimation of structure diversity. Using an interdisciplinary 15 approach combining physics and biology, we here quantify the colour and structure of 36 hummingbirds species evenly 16 distributed across the phylogeny. We explore at least 2 patches per species, which are assumed to be under different 17 selective regimes. For each patch, we measure structural features (number of layers, layer width, irregularity, spacing, 18 etc.) of the feathers at different scales using both optical and electronic microscopy and we measure colour using a 19 novel approach we developed to encompass the full complexity of iridescence, including its angular dependency. We 20 discover an unsuspected diversity of structures producing iridescence in hummingbirds. We also study the effect of 21 several structural features on the colour of the resulting signal, using both an empirical and modelling approach. Our 22 findings demonstrate the need to take into account multiple patches per species and suggest possible evolutionary 23 pressures causing the evolutionary transitions from one melanosome type to another. 24 Hummingbirds are famous for their bright and shiny colours which change with the illumination or observation 26 angle: a phenomenon known as iridescence. Iridescent colours are produced by the interaction of light with periodic 27 nanometre-scale structures such as multilayers or diffraction gratings and are widespread among many taxa [1]. But few 28 taxa display colours as bright and as saturated as the hummingbirds (Trochilidae family). Most hummingbird species 29 harbour two visually distinct types of iridescent colour patches, as illustrated in fig. S1: directional patches, which are 30 only visible at a very narrow angle range [2] and are often very bright and saturated, and diffuse patches, for which 31 some colour is visible from any angle [2] and that are often not as bright as directional patches. Directional patches are 32 often located on facial or ventral patches and thought to be involved in communication while diffuse patches are often 33 located on dorsal patches and thought to be involved in camouflage [3]. Additionally, although all hummingbird species 34 display some degree of iridescence, striking differences can be noticed between the various species and body patches in 35 terms of brightness (describing how much light is reflected by the object), saturation (describing the colour "purity") 36 and directionality [4]. 37Yet, the structural bases of this intra-individual and interspecific diversity...

Evolution of brilliant iridescent feather nanostructures

“…Moreover, our results suggest that there would be little or no difference in brightness between structures with solid platelets and hollow platelets (only between thin rods and hollow and/or platelet-shaped melanosomes), which is the variability we see in hummingbirds. Indeed, Gruson et al, 2019 found color production to be similar among patches with different melanosome types in hummingbirds. We speculate that high variability in melanosome type in hummingbirds and birds-of-paradise is not related to general optical benefits of specific melanosome types or modifications, but rather to general high rates of color change in these groups (Eliason et al, 2020;Parra, 2010).…”

“…Hummingbirds, whose iridescent structures are typically built with hollow platelets, can also exhibit interpatch variability in melanosome type. Some patches may contain a structure with solid platelets, or even mixed structures with both hollow and solid platelets (Gruson et al, 2019). It is notable that the only known examples of interpatch variability in melanosome type comes from the birds-of-paradise and hummingbirds-groups that are known to have exceptionally high rates of color evolution (Eliason et al, 2013;Ligon et al, 2018;Parra, 2010).…”

“…With few exceptions, most studies sampled only a single iridescent patch from each species. This is based on the assumption that iridescent nanostructures are similar in all iridescent patches in a species, which seems to be true in most species but not all; hummingbirds and birds-of-paradise are the only known exceptions (Durrer, 1977; Gruson et al, 2019).…”

“…While previous studies focusing on nanostructural evolution and color-producing mechanisms in a variety of avian subclades (Eliason et al, 2020(Eliason et al, , 2015(Eliason et al, , 2013Eliason and Shawkey, 2012;Gammie, 2013;Gruson et al, 2019;Maia et al, 2013b;Quintero and Espinosa de los Monteros, 2011) have given us valuable insights into the evolution and optics of iridescent structures, they have focused on specific species, subclades or a particular melanosome type in isolation. Thus, they have not uncovered the broader, general principles governing the evolution of brilliant iridescent plumage, and several key questions remain unanswered.…”

Engineering with keratin: A functional material and a source of bioinspiration

“…Besides the outstanding mechanical, lightweight, and thermal properties of avian feathers, these keratinous materials are also known to display a diverse range of vibrant colors. This property is in part due to structural coloration, which arises from the interactions of light with a submicron array of varying morphologies which include multilayer structures (as seen in the iridescent throat patch of the hummingbird) ( Gruson et al., 2019 ), two-dimensional photonic crystals (as seen in peacock and mallard feathers) ( Freyer and Stavenga, 2020 ; Stavenga et al., 2017 ; Weiss and Kirchner, 2010 ; Zi et al., 2003 ), or spinodal-like channel structures ( Parnell et al., 2015 ) (as seen in the Eurasian Jay Garrulus glandarius ). These nanostructures self-assemble and can occur as a multi-layered structure of β-keratin and a pigment-based protein (e.g., melanin, carotenoids), as shown in Figure 18 A.…”