Carotenoids produce most of the brilliant orange and yellow colours seen in animals, but animals cannot synthesize these pigments and must rely on dietary sources. The idea that carotenoids make good signals because they are a scarce limiting resource was proposed two decades ago and has become the leading hypothesis for the role of carotenoids in animal communication. To our knowledge, until now, however, there has been no direct evidence that carotenoids are a limiting resource in nature. We showed that carotenoid availability in the wild limits the expression of sexual coloration in guppies (Poecilia reticulata), a species in which females prefer males with brighter orange carotenoid-containing spots. Further, the degree of carotenoid limitation varies geographically along a replicated environmental gradient (rainforest canopy cover), which opens new avenues for testing signal evolution theory.
Carotenoid-based sexual coloration is the classic example of an honest signal of mate quality. Animals cannot synthesize carotenoid pigments and ultimately depend on dietary sources. Thus, in carotenoidpoor environments, carotenoid coloration may be a direct indicator of foraging ability and an indirect indicator of health and vigour. Carotenoid coloration may also be a¡ected, more directly, by parasites in some species. Carotenoids are not, however, the only conspicuous pigments available to animals. Pteridine pigments, with similar spectral properties, are displayed in the exoskeletons and wings of insects, the irides of birds and the skins of ¢shes, lizards and amphibians. Unlike carotenoids, pteridines are synthesized de novo by animals. We report that the orange spots that male guppies (Poecilia reticulata) display to females contain red pteridine pigments (drosopterins) in addition to carotenoids. We also examined the relationship between drosopterin production by males and carotenoid availability in the ¢eld. The results contrasted sharply with the hypothesis that males use drosopterins to compensate for carotenoid scarcity: males used more, not less, drosopterins in streams with higher carotenoid availability. The positive association between drosopterin use and carotenoid availability could re£ect the costs of drosopterin synthesis or it could be a consequence of females preferring a particular pigment ratio or hue. Male guppies appear to use drosopterin pigments in a manner that dilutes, but does not eliminate, the indicator value of carotenoid coloration.
Abstract. Trinidad guppies (Poecilia reticulata) are distributed along an environmental gradient in carotenoid availability that limits the carotenoid content of the orange spots of males. The amount of synthetic red pteridines (drosopterins) in the orange spots covaries with the carotenoid content, such that the ratio of the two types of pigments is roughly conserved across streams. Carotenoids and drosopterins have different spectral properties and thus the ratio of the two types of pigments affects the shape of the orange spot reflectance spectrum. Geographic conservation of the carotenoid:drosopterin ratio suggests that males may be under selection to maintain a particular hue. We tested this hypothesis by comparing the pigmentation and coloration of guppies from six streams in the field to that of second-generation descendants of the same populations raised on three dietary carotenoid levels in the laboratory. The results show clearly that the geographic variation in drosopterin production is largely genetic and that the hue of the orange spots is conserved among populations in the field, relative to the laboratory diet groups. This is a countergradient pattern because genetic differences between populations in drosopterin production mask the effect of carotenoid availability on the hue of the orange spots. The potential for countergradient sexual selection to contribute to reproductive isolation between populations is discussed.
I used spectrophotometric, chromatographic, and chemical means to establish that rhodoxanthin, a 3-keto-retrodehydro carotenoid, was the only red pigment in the head feathers of the Western Tanager (Piranga ludoviciana). In contrast, the red head and body feathers of a close relative, the Scarlet Tanager (P. olivacea), exhibited several 4-keto-carotenoids. Other tanagers and emberizids also displayed 4-keto-carotenoids. The deposition of presumed canary xanthophylls and phaeomelanins differed quantitatively between the Western Tanager and other tanagers belonging to the genus Piranga. Uniquely among the Piranga spp. examined, the head feathers of the Western Tanager had flattened bards without barbules. Partly because the head colors of the Western and Scarlet tanagers were indistinguishable either in the hand or when examined by reflectance spectrophotometry, I excluded selection for a variant color as the basis for the observed chemical and morphological differences. Biochemical costs, including putative costs associated with the endogenous production of 4-keto-carotenoids, could have led to the conversion in the Western Tanager to an available dietary pigment. This tanager, unlike the other species studied, has access to an abundant source of rhodoxanthin in the coniferous forests of western North America. The pigment changes in the Western Tanager could have taken place with minimal effect on head color.
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