A Review and Assessment of the Shared-Pathway Hypothesis for the Maintenance of Signal Honesty in Red Ketocarotenoid-Based Coloration

Abstract

For decades, scientists have noted connections between individual condition and carotenoid-based coloration in terrestrial and aquatic animals. Organisms that produce more vibrant carotenoid-based coloration tend to have better physiological performance and behavioral displays compared to less colorful members of the same species. Traditional explanations for this association between ornamental coloration and performance invoked the need for color displays to be costly, but evidence for such hypothesized costs is equivocal. An alternative explanation for the condition-dependence of carotenoid-based coloration, the Shared-Pathway Hypothesis, was developed in response. This hypothesis proposes that red ketocarotenoid-based coloration is tied to core cellular processes involving a shared pathway with mitochondrial energy metabolism, making the concentration of carotenoids an index of mitochondrial function. Since the presentation of this hypothesis, empirical tests of the mechanisms proposed therein have been conducted in many species. In this manuscript, we review the Shared-Pathway Hypothesis and the growing number of studies that have investigated a connection between carotenoid-based coloration and mitochondrial function. We also discuss future strategies for assessing the Shared-Pathway Hypothesis to more effectively disentangle evidence that may simultaneously support evidence of carotenoid-resource tradeoffs.

The evolution of carotenoid‐based plumage colours in passerine birds

“…The length of the metabolic path is the maximum number of enzymatic reactions from dietary to expressed carotenoids, and was obtained from an exhaustive survey (Morrison & Badyaev, 2016). Carotenoids produced by longer metabolic pathways are more resistant to degradation (Higginson et al, 2016), and potentially more strongly linked to cellular respiration (Powers & Hill, 2021). Data included 187 passerine species with carotenoid‐based coloration of which 116 had red and 71 had only yellow (both sexes combined as metabolic data is not sex‐specific).…”

“…Instead, it has been suggested that only some types of carotenoid‐based coloration constitute honest signals of quality, namely colours that are caused by the deposition of metabolically modified carotenoids (which are often red). This hypothesis comes from the observation that the metabolic pathway to produce these colours is coupled directly with key aspects of cellular physiology, specifically mitochondrial respiration (Hill, 2011; Powers & Hill, 2021). Meta‐analyses have supported this argument by demonstrating that ornamentation based on metabolically derived carotenoids is a better indicator of individual quality than ornamentation based on unmodified dietary carotenoids (Weaver et al, 2018).…”

Relocation to avoid costs: A hypothesis on red carotenoid‐based signals based on recent CYP2J19 gene expression data

“…[19,25] This shared mechanism would lead to a close-fitting association between the level of expression of the signaling trait and overall mitochondrial function. [26] Assuming that mitochondrial functioning is key for many critical cell processes, the trait would become intrinsically linked to individual quality. [26] Hence, its production would not be subject to resource allocation trade-offs that, in turn, generate production costs.…”

“…[26] Assuming that mitochondrial functioning is key for many critical cell processes, the trait would become intrinsically linked to individual quality. [26] Hence, its production would not be subject to resource allocation trade-offs that, in turn, generate production costs. [17] Similarly, it would neither generate any direct cost (damage), such as initially formulated for the overall reproductive investment (i.e., [27,28] ).…”

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“…Indeed, a deficiency in ATP can be compensated for through many different changes in mitochondrial dynamics [87][88][89][90][91]. Even though these ideas are largely speculative, a positive relationship between the metabolic rate and astaxanthin bioconversion has been observed in hybrid T. californicus [92]. In wild male house finches, individuals with greater energetic capacity are better able to bioconvert carotenoids [26].…”