Tissue structure contributes to the production of a coloured skin display in the Common Myna

Abstract

Conspicuous coloured displays from ultraviolet to bright red have been documented in many species throughout the animal kingdom. These colours often occur as sexual signals and can be incorporated into different types of integuments (e.g. scales, feathers, skin). Two main mechanisms are known to produce coloured integuments: pigmentation and tissue structure. Although pigmental and structural coloration are separate mechanisms and can occur independently, some coloured displays might emerge from a combination of both. Here, we demonstrate, using biochemical, optical and morphological methodologies, that the yellow coloration of the skin located around the eye of Common (Indian) Mynas ( Acridotheres tristis) is produced by both light-reflecting nanostructures and light-absorbing carotenoid pigments. Our analysis confirms that nanostructured collagen in the avian dermis work in combination with carotenoid pigments to produce vivid integumentary colours. Identifying the mechanisms behind the production of a coloured signal provides a basis for predicting how a signal’s function might be influenced by environmental factors such as fledgling nutrition.

Identifying and locating carotenoids in supra‐orbital combs of male black grouse (Lyurus tetrix) using Raman and transmission electron microscopy: A histological study using rehydrated tissue samples

“…As the anatomy of dermal spikes of black grouse specifically was unknown, structures were identified through similar tissue comparison, such as that of the chicken comb and wattle and coloured skin patches of Cabot's tragopan and the common myna (Lucas & Stettenheim, 1972; Nakano et al, 1996; Peneaux et al, 2020; Prum & Torres, 2003; Yoshioka et al, 2010) among others, and implementing a variety of stains and microscopy techniques. The stratum corneum is always easily identifiable due to its characteristic “plate and mortar” appearance (Burton, 1976; Elias et al, 1987; Peneaux et al, 2020; Prum & Torres, 2003), however, the thickness of this layer greatly differs between samples. Time spent in storage and the rehydration process may have affected this, however, the adapted rehydration methods used have been used previously, with a huge level of success (Chen et al, 2017; Mekota & Vermehren, 2005; Schmidt et al, 2000).…”

“…Skin colours often arise from epidermal tissue in a variety of ways. Pigments can be synthesised by organelles, such as melanosomes within melanocytes found in the basal layer of the epidermis (Khumpeerawat et al, 2021), be deposited within the epidermis in lipid‐filled cells (Menon & Menon, 2000; Peneaux et al, 2020), or be contained within specialised neuromuscular organs, such as chromatophores in Cephalopods located between the transparent epidermal layer and the reflective iridophore layer within the skin (Kirkwood et al, 2013; Messenger, 2001). Additionally, colours can be produced or enhanced by the presence of structural colours (Iverson & Karubian, 2017; Justyn et al, 2022; Stettenheim, 2000; Stoddard & Prum, 2011).…”

“…Though birds use mainly plumage‐based colouration (Cooney et al, 2019; Dale et al, 2015) bare‐skin signals are also widespread and include coloured eye rings (Pérez‐Rodríguez & Viñuela, 2008), coloured legs and feet (Torres & Velando, 2005) and wattles and eye combs (Harris et al, 2018). Despite showing variation in size, colour or structure, bare skin signals have received less attention than colourful plumage displays (Iverson & Karubian, 2017), with only a handful of studies examining the internal structures and underlying anatomy of skin‐based signals (e.g., (Negro et al, 2006; Peneaux et al, 2020; Prum & Torres, 2003) despite their importance in intra‐ and interspecies communication.…”

“…Colours in animals are typically the result of two broad mechanisms, either acting individually or in combination (Mills & Patterson, 2009). First, pigment molecules can be incorporated within layers of the skin or embedded into the feather or hair fibre on top of a reflective base layer (Mougeot et al, 2007; Peneaux et al, 2020; Prum & Torres, 2003) producing colour through the absorption and reflection of specific wavelengths, with colour saturation often depending on the concentration of pigment molecules (Galván & Solano, 2016; Maia et al, 2009; Pike et al, 2011). Most commonly these pigments are melanins, producing blacks, browns and rufous reds (McGraw et al, 2004; McGraw, 2006), while brighter colours, such as yellows, oranges and reds are often produced through the incorporation of dietary carotenoids (García‐de Blas et al, 2013; Peneaux et al, 2020; Peters et al, 2004).…”

“…First, pigment molecules can be incorporated within layers of the skin or embedded into the feather or hair fibre on top of a reflective base layer (Mougeot et al, 2007; Peneaux et al, 2020; Prum & Torres, 2003) producing colour through the absorption and reflection of specific wavelengths, with colour saturation often depending on the concentration of pigment molecules (Galván & Solano, 2016; Maia et al, 2009; Pike et al, 2011). Most commonly these pigments are melanins, producing blacks, browns and rufous reds (McGraw et al, 2004; McGraw, 2006), while brighter colours, such as yellows, oranges and reds are often produced through the incorporation of dietary carotenoids (García‐de Blas et al, 2013; Peneaux et al, 2020; Peters et al, 2004). Second, structural colours—typically responsible for ultraviolet, blues, white and iridescent colours in birds—arise through either constructive or deconstructive interference of light with ordered or disordered nanostructures within the skin (Prum & Torres, 2003; Shawkey & D'Alba, 2017), rather than deposited pigments (McGraw et al, 2002; Prum & Torres, 2003).…”