A call to integrate non-visual functions of pigments and their interactions with visual functions to understand global change impacts on visual systems

1 INTRODUCTION

Vision plays a central role in the ecology of many organisms, shaping the outcomes of their interactions with each other and the environment (e.g. predator–prey; host–parasite). The evolution of visual systems is impacted by variation in visual traits (e.g. coloration; Endler et al., 2005), which can have signalling roles but which may also have non-signalling functions that have significant and synergistic effects (Koneru & Caro, 2022). Importantly, animal coloration, which derives from diverse pigments and structures and is shaped by numerous biotic and abiotic factors, occurs in both integumentary structures (i.e. skin, fur, feathers, beaks, scales and shells), and non-integumentary structures (i.e. inner organs and blood; Hill & McGraw, 2006). Because integumentary structures are the component that interacts directly with the environment, this is the tissue that is most likely to have an impact on the evolution of visual systems and is thus the focus of this perspective. To date, substantial progress has been made on our understanding of how organisms detect visual cues including the precise estimations of colour vision and visual capabilities (e.g. Maia et al., 2019; van den Berg et al., 2020; Vorobyev & Osorio, 1998) and how specific visual systems may be influenced by their environments (e.g. Endler, 1992; Härer et al., 2018; Leal & Fleishman, 2002). However, given the range of pigmented integumentary tissues that occur in nature (Figure 1), there is still much to learn about the non-visual functional significance of these pigments and how they may subsequently influence visual systems, particularly as global change alters selective landscapes (Koneru & Caro, 2022; Rojas, 2016).

FIGURE 1

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Pigments are used to make the wide variety of animal coloration displayed here. Pigments used for signals have to date been given the most attention for the likely impacts of global change on their display. However, many of the pigments above actually have non-visual or unknown functions. (a) The function of the low and high melanin concentrations in the, respectively, light and dark polymorphs of these timber rattlesnakes (Crotalus horridus) are unknown. (b) The dark melanins of the wood tiger moth (Parasemia plantaginis) aid in thermoregulation but reduce the warning signal created by the contrast between melanins and the yellow colour. (c) The barred owl (Strix varia) feather has melanized (dark) and un-pigmented (white) sections. (d) The bright red skin of the northern red salamander (Pseudotriton ruber) advertises its toxicity as a part of a Müllerian mimicry group. (e) The blue colour created by biliverdin in these eastern blue bird (Sialia sialis) eggs is hypothesized to have a thermoregulatory function in some species because biliverdin reflects near infrared wavelengths. (f) The seemingly obvious orange morph of the brown anole (Anolis sagrei) is more cryptic than the brown morph to bird predators. (g) The orange belly of the harlequin toad (Atelopus aff. franciscus) has an unknown function. (h) The bright orange colours on the plastron of the painted turtle (Chrysemys picta) are attributed to stored carotenoids that may be moved into the bloodstream to counteract oxidative stress during recovery from overwintering stress. (i) The pigmented bib and mask of the common yellowthroat (Geothlypis trichas) are used as signals to advertise quality. Photo credits: Julian Avery (a, c, d, e, i), Beth Reinke (f, h), Bibiana Rojas (g), Wikimedia Commons (b: Charles J. Sharp).

As human impacts increase, natural ecosystems are expected to face a diversity of pressures associated with environmental change (i.e. pollutants and habitat alteration) that may influence pigmentation and coloration (Delhey & Peters, 2017; Koneru & Caro, 2022). Increased extreme temperature variability associated with global climate change may decouple coevolved pigment and pattern relationships leading to important functional and ecological consequences. For example, heat and cold shocks during butterfly development have been shown to uncouple pigments from pattern formation in adults, resulting in potentially maladaptive displays (Connahs et al., 2016). Similarly, artificial light at night can change amphibian coloration and, importantly, the ability for some amphibian species to match their backgrounds (Horn et al., 2023). An important limitation in our understanding of how environmental change influences visual ecology is that research tends to consider cases where colour is a trait that performs a known function, such as when it is used for communication, camouflage or thermoregulation (e.g. Delhey & Peters, 2017; Zimova et al., 2016). In these cases, selective pressures act directly on coloration (Figure 2). In contrast, while relevant to animal fitness and survival, the effects of the environmental change on pigments with functions such as antioxidation, support and physical protection have rarely been considered. The physiology, complex nature and functional obscurity of many pigments often prevent evolutionary ecologists from incorporating this information into studies of coloration. In this perspective piece, we argue for the need to consider the myriad functions of pigments themselves when making predictions about species' responses to global change, and the subsequent impacts on visual systems, because the functional significance of the pigment will determine which traits selection affects (Figure 2). Despite the past research bias towards visually adaptive signals, it is important to acknowledge that there are likely many unknown non-visual roles and synergistic effects of pigments involved in organismal responses to global change.

FIGURE 2

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Theoretical framework illustrating how global change can impact colour and visual system evolution. Coloration can be made by pigments (specific biomolecules), structure (tissue that differentially reflect wavelengths of light) or a combination of the two. Selection will act on coloration in cases where the colour is used for communication, camouflage or thermoregulation and will act directly on pigments when the pigments are used for antioxidation, detoxification, structural support or protection. The strength and direction of the selective pressure on either or both traits may be altered by the modifiers. Changes to an organism's coloration will then impact the colour trait distribution of the ecosystem, which may also have impacts on visual systems of species within the ecosystem (intended receivers, predators, etc.).

To address these gaps in our understanding of the functions of pigmentation and coloration, and their subsequent impacts on visual systems in the face of global change (defined as any human-induced environmental change), we will (1) summarize the main functions pigments can have in integument with a focus on non-visual roles, (2) provide an overview of how global change could impact coloration and pigmentation, (3) discuss some of the known modifiers between pigment functions and their interactions with global change and (4) connect these changes in colour traits to possible subsequent visual system evolution. Though both structural elements and pigments contribute to animal coloration (Figure 2), we focus here on pigments. Throughout this perspective, we highlight select examples that illustrate exciting directions in coloration research and where possible, we point the reader towards useful and insightful reviews.