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    Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade‐off hypothesis proposes that condition‐dependent honest signalling relies on a trade‐off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re‐allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition‐dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition‐dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.

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    The shared-pathway hypothesis offers a cellular explanation for the connection between ketocarotenoid pigmentation and individual quality. Under this hypothesis, ketocarotenoid metabolism shares cellular pathways with mitochondrial oxidative phosphorylation such that red carotenoid-based coloration is inextricably linked mitochondrial function. To test this hypothesis, we exposed Tigriopus californicus copepods to a mitochondrially targeted protonophore, 2,4-dinitrophenol (DNP), to induce proton leak in the inner mitochondrial membranes. We then measured whole-animal metabolic rate and ketocarotenoid accumulation. As observed in prior studies of vertebrates, we observed that DNP treatment of copepods significantly increased respiration and that DNP-treated copepods accumulated more ketocarotenoid than control animals. Moreover, we observed a relationship between ketocarotenoid concentration and metabolic rate, and this association was strongest in DNP-treated copepods. These data support the hypothesis that ketocarotenoid and mitochondrial metabolism are biochemically intertwined. Moreover, these results corroborate observations in vertebrates, perhaps suggesting a fundamental connection between ketocarotenoid pigmentation and mitochondrial function that should be explored further.

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  3. Dam, Hans G. (Ed.)
    The marine copepod, Tigriopus californicus , produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T . californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success. 
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  4. Abstract Quantifying variation in the ability to fight infection among free-living hosts is challenging and often constrained to one or a few measures of immune activity. While such measures are typically taken to reflect host resistance, they can also be shaped by pathogen effects, for example, if more virulent strains trigger more robust immune responses. Here, we test the extent to which pathogen-specific antibody levels, a commonly used measure of immunocompetence, reflect variation in host resistance versus pathogen virulence, and whether these antibodies effectively clear infection. House finches ( Haemorhous mexicanus ) from resistant and susceptible populations were inoculated with > 50 isolates of their novel Mycoplasma gallisepticum pathogen collected over a 20-year period during which virulence increased. Serum antibody levels were higher in finches from resistant populations and increased with year of pathogen sampling. Higher antibody levels, however, did not subsequently give rise to greater reductions in pathogen load. Our results show that antibody responses can be shaped by levels of host resistance and pathogen virulence, and do not necessarily signal immune clearance ability. While the generality of this novel finding remains unclear, particularly outside of mycoplasmas, it cautions against using antibody levels as implicit proxies for immunocompetence and/or host resistance. 
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  5. Synopsis 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 with 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 (SPH), 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 several species. In this manuscript, we review the SPH 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 SPH to more effectively disentangle evidence that may simultaneously support evidence of carotenoid-resource tradeoffs. 
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  6. null (Ed.)