Seasonal but not sex-biased gene expression of the carotenoid ketolase, CYP2J19, in the sexually dichromatic southern red bishop (Euplectes orix)

Abstract

Intense red colours in birds are often owing to ketocarotenoids (KCs). In many land birds, KCs are oxidized from dietary yellow precursors, presumably by the avian carotenoid ketolase CYP2J19, the regulation and constraints of which have important implications for condition-dependence and honest signalling of carotenoid colour displays. We investigated hepatic CYP2J19 gene expression in the seasonally and sexually dichromatic southern red bishop (Euplectes orix) in relation to season, sex, progression of the prenuptial moult, testis size, body condition, redness and circulating sex steroids. A coloration function of CYP2J19 is supported by a seasonal upregulation prior to and during the carotenoid-depositing stage of the male prenuptial moult. However, CYP2J19 expression was similarly high in females (which do not moult prenuptially), and remained high in males after moult, suggesting additional or alternative roles of hepatic CYP2J19 or its products, such as detoxification or antioxidant functions. In males, the CYP2J19 upregulation preceded and was unrelated to the rise in plasma testosterone, but was correlated with androstenedione, probably of adrenal origin and compatible with luteinizing hormone-induced and (in females) oestrogen-suppressed moult. Finally, contrary to ideas that carotenoid ketolation rate mediates honest signalling of male quality, CYP2J19 expression was not related to plumage redness or male body condition.

Keywords: CYP2J19; androstenedione; carotenoid metabolism; ketocarotenoids; plumage coloration; testosterone.

Figure 1.

Prenuptial moult stages in male southern red bishops: CARD, before or during carotenoid deposition in feathers; PostCARD, after completed carotenoid deposition (see methods for detailed criteria). (a) CARD male in pre-breeding plumage just prior to moult start, still indistinguishable from female and non-breeding male plumage. (b) CARD male with ongoing carotenoid deposition in emerging collar feathers. (c) A fully nuptial PostCARD male. (d) Growing rump feathers, some with ongoing (pins or just emerged vane) and some with completed carotenoid deposition. (e) Fully nuptial plumage on a PostCARD male, with fully grown rump and collar feathers in the inset picture (f).

Figure 2.

CYP2J19 expression in relation to (a) season, (b) sex (during the breeding season), and (c) reproductive development. (a,b) Raw values are represented by circles (males) or triangles (females). Boxplots show median, first and third quantiles with whiskers extending no further than 1.5 times the inter-quartile range. Horizontal jitter was added to improve visualization of individual data points. (c) Raw values are represented by black (CARD) or white (PostCARD) circles. Lines represent the linear model fit for CARD (solid line) and PostCARD (dashed line) males. Testis length was scaled within each prenuptial moult stage, to allow comparison between categories (see the electronic supplementary material, figure S1 for an unscaled version of the plot). In all plots, normalized CYP2J19 expression values are square root transformed. ***p < 0.001.

Figure 3.

Relationship between androstenedione (A4) titre and (a) CYP2J19 expression and (b) testosterone (T) titre. Raw values are represented by black (CARD) or white (PostCARD) circles. Lines represent least-squares regressions for CARD (solid line) and PostCARD (dashed line) males. Normalized CYP2J19 expression is square root transformed.