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The carotenoid-based ornaments displayed by many birds often play key roles in social and sexual signalling, revealing information about individual quality. However, the proximate regulation of the honesty of sexual traits remains controversial. Understanding the mechanisms of coloured trait production and maintenance requires an accurate description of their chemical composition and of the physiological pathways involved in pigment production and deposition in the ornaments. Carotenoid-based colouration has been extensively studied in birds, but such information is often lacking for coloured integuments other than feathers, such as fleshy carotenoid-based ornaments. Here we report the carotenoid composition of the combs of the red grouse (Lagopus lagopus scoticus), a sexual trait that honestly reveals individual quality. In the present study, we also investigated blood carotenoid content, as well as associations between carotenoids, retinol and tocopherol (the active forms of vitamin A and E, respectively) within the ornament. We found that comb pigmentation was primarily the result of two red ketocarotenoids (astaxanthin and papilioerythrinone), which are synthesised from their dietary precursors (zeaxanthin and lutein) directly at the comb integument. These red ketocarotenoids are largely deposited esterified with fatty acids. Astaxanthin concentration in the comb was found to negatively correlate with retinol levels but positively correlate with tocopherol levels. Considering evidence from this and other studied species, we suggest that carotenoid esterification is a characteristic of coloured fleshy integuments, probably affecting pigment stability and colouration in living tissues, with subsequent effects on their signalling role and maintenance costs. We found little evidence that the honesty of this signal would result from a direct connection with vitamin A metabolism, as recently proposed. Rather, honest signalling via comb colouration appears more related to potential allocation trade-offs of some specific dietary precursors or to the capacity of individuals to manage the redox reactions interfering with carotenoid metabolism., This study was financed in part by project CGL2011-26318 (Ministerio de Ciencia e Innovación). LP-R was supported by a postdoctoral contract from the Spanish Ministerio de Economía y Competitividad (MINECO), through the Severo Ochoa Programme for Centres of Excellence in Research, Development and Innovation (SEV-2012-0262).