Many of the colour displays of animals are proposed to have evolved in response to female mate choice for honest signals of quality, but such honest signalling requires mechanisms to prevent cheating. The most widely accepted and cited mechanisms for ensuring signal honesty are based on the costly signalling hypothesis, which posits that costs associated with ornamentation prevent low-quality males from being highly ornamented. Alternatively, by the index hypothesis, honesty can be achieved via cost-free mechanisms if ornament production is causally linked to core physiological pathways. In this essay, we review how a costly signalling framework has shaped empirical research in mate choice for colourful male ornaments and emphasize that alternative interpretations are plausible under an index signalling framework. We discuss the challenges in both empirically testing and distinguishing between the two hypotheses, noting that they need not be mutually exclusive. Finally, we advocate for a comprehensive approach to studies of colour signals that includes the explicit consideration of cost-free mechanisms for honesty.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.
Yellow, orange, and red coloration is a fundamental aspect of avian diversity and serves as an important signal in mate choice and aggressive interactions. This coloration is often produced through the deposition of diet-derived carotenoid pigments, yet the mechanisms of carotenoid uptake and transport are not wellunderstood. The white recessive breed of the common canary (Serinus canaria), which carries an autosomal recessive mutation that renders its plumage pure white, provides a unique opportunity to investigate mechanisms of carotenoid coloration. We carried out detailed genomic and biochemical analyses comparing the white recessive with yellow and red breeds of canaries. Biochemical analysis revealed that carotenoids are absent or at very low concentrations in feathers and several tissues of white recessive canaries, consistent with a genetic defect in carotenoid uptake. Using a combination of genetic mapping approaches, we show that the white recessive allele is due to a splice donor site mutation in the scavenger receptor B1 (SCARB1; also known as SR-B1) gene. This mutation results in abnormal splicing, with the most abundant transcript lacking exon 4. Through functional assays, we further demonstrate that wild-type SCARB1 promotes cellular uptake of carotenoids but that this function is lost in the predominant mutant isoform in white recessive canaries. Our results indicate that SCARB1 is an essential mediator of the expression of carotenoid-based coloration in birds, and suggest a potential link between visual displays and lipid metabolism.coloration | carotenoids | lipid metabolism | Serinus canaria T he yellow, orange, and red coloration of the feathers, skin, and beaks of birds is most commonly produced through the deposition of carotenoid pigments (1). Carotenoid coloration of birds has been a focus of study in the fields of behavior, evolution, and physiology because it plays a key role in mate assessment in many species. In addition, it is frequently an indicator of individual quality, and can signal species identity (2-4). Birds cannot synthesize carotenoids de novo and must acquire them through their diet (1), potentially linking coloration to the acquisition of pigments from the environment (3). Thus, key hypotheses related to honest signaling and sexual selection have been shaped by and are currently being tested in carotenoidornament systems (5, 6). Ultimately, the information content and evolutionary trajectories of carotenoid ornaments are a function of the physiological mechanisms underlying color expression, yet our understanding of these mechanisms is limited.The expression of carotenoid coloration in birds involves four distinct physiological steps: uptake in the gut, transport in circulatory and lymphatic systems, metabolism either at the site of deposition or in the liver, and deposition in the integument (7). Recent progress has been made in understanding how carotenoids are metabolized to novel forms. In 2016, two studies independently identified a key carotenoid metabolism enzyme,...
Understanding the mechanisms that link ornamental displays and individual condition is key to understanding the evolution and function of ornaments. Immune function is an aspect of individual quality that is often associated with the expression of ornamentation, but a general explanation for why the expression of some ornaments seems to be consistently linked to immunocompetence remains elusive. We propose that condition-dependent ornaments may be linked to key aspects of immunocompetence through co-dependence on mitochondrial function. Mitochondrial involvement in immune function is rarely considered outside of the biomedical literature, but the role of mitochondria as the primary energy producers of the cell and the centres of biosynthesis, the oxidative stress response, and cellular signalling place them at the hub of a variety of immune pathways. A promising new mechanistic explanation for correlations between a wide range of ornamental traits and the properties of individual quality is that mitochondrial function may be the 'shared pathway' responsible for links between ornament production and individual condition. Herein, we first review the role of mitochondria as both signal transducers and metabolic regulators of immune function. We then describe connections between hormonal pathways and mitochondria, with implications for both immune function and the expression of ornamentation. Finally, we explore the possibility that ornament expression may link directly to mitochondrial function. Considering condition-dependent traits within the framework of mitochondrial function has the potential to unify central tenets within the study of sexual selection, eco-immunology, oxidative stress ecology, stress and reproductive hormone biology, and animal physiology.
Summary1. Physiological ecologists require techniques for controlled oxidative challenges in live animals to facilitate the study of oxidative stress. 2. Techniques for manipulating oxidative stress include agents that increase generation of pro-oxidants, such as paraquat, diquat, radiation, heavy metals, dietary oxidized lipids, and tert-butyl-hydroperoxide, as well as genetic (RNAi) and chemical (buthionine sulfoximine) knock-downs that target specific antioxidants. 3. We critically assess both currently used and potentially useful methods for inducing systemic oxidative challenge in animals. We provide a resource for biologists to select the most robust methods for oxidative challenge in their study system, to improve interpretation of results within the context of cellular mechanisms and to maximize effectiveness of experiments while minimizing unintended side effects.
Abstract1. Within the past several decades, resource trade-offs have emerged as the commonly accepted explanation for how carotenoid-based coloration links to individual performance. However, the literature on carotenoid signalling is inconsistent in how carotenoid resource trade-offs are defined, assessed and interpreted.2. We provide a clear statement of the resource trade-off hypothesis for explaining the honesty of carotenoid-based ornaments, its key assumptions and evidence for (or against) each assumption.3. Focusing on class Aves, we perform a critical assessment of theoretical and empirical evidence for carotenoid resource limitation and for direct physiological benefits of carotenoid pigments to immune and antioxidant performance.4. We identify important inconsistencies in how data related to physiological function and carotenoid coloration have been interpreted in the light of the resource trade-off hypothesis, and we suggest directions for future research. K E Y W O R D Santioxidants, carotenoid pigments, coloration, ornamentation | 1909Functional Ecology KOCH and HILL Comparisons among classes of vertebrates or between verte-brates and invertebrates can provide important insights, but tackling physiological differences among major taxonomic groups further complicate an already complex topic. By focusing on birds in this review, we hope to highlight patterns and questions that will have important implications for other taxa, and we encourage application of the questions raised here to other systems.In this review, we assess trade-off mechanisms proposed to explain honest signalling in carotenoid-coloured ornaments while also considering evidence for the direct physiological benefits of carotenoids to the individual. In the process of evaluating the current state of understanding of the main assumptions of the carotenoid resource trade-off hypothesis, we examined 179 empirical studies of carotenoid-based traits in birds published between 1992 and 2017; we provide a list of these studies for reference (Supporting Information Table S1, Appendix S1, Figures S1 and S2 for more detail). While debates regarding the physiological benefits of carotenoids or whether carotenoids are limited resources are not new, here, we focus on a specific, unifying framework and its main predictions. We highlight where assessment can be made based on currently available data and highlight where more information is needed to adequately test the carotenoid resource trade-off hypothesis. | A SSUMP TI ON 1: C AROTENOID LI M ITATI O NWithout carotenoid limitation, carotenoid resource trade-offs cannot be the basis for honest signalling in carotenoid-based traits.Thus, the question of whether carotenoids are limiting resources for birds is a central question related to the resource trade-off hypothesis in avian species (Hadfield & Owens, 2006;Hill, 1994;Hudon, 1994;Olson & Owens, 1998;Simons, Maia, Leenknegt, & Verhulst, 2014). An important distinction is that carotenoid limitation can be interpreted from two distinct perspectives:...
Dietary carotenoids have been proposed to boost immune system and antioxidant functions in vertebrate animals, but studies aimed at testing these physiological functions of carotenoids have often failed to find support. Here we subject yellow canaries (Serinus canaria), which possess high levels of carotenoids in their tissue, and white recessive canaries, which possess a knockdown mutation that results in very low levels of tissue carotenoids, to oxidative and pathogen challenges. Across diverse measures of physiological performance, we detect no differences between carotenoid-rich yellow and carotenoid-deficient white canaries. These results add further challenge to the assumption that carotenoids are directly involved in supporting physiological function in vertebrate animals. While some dietary carotenoids provide indirect benefits as retinoid precursors, our observations suggest that carotenoids themselves may play little to no direct role in key physiological processes in birds.
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