Ecological effects on female bill colour explain plastic sexual dichromatism in a mutually-ornamented bird

Abstract

Sex differences in ornamentation are common and, in species with conventional sex roles, are generally thought of as stable, due to stronger sexual selection on males. Yet, especially in gregarious species, ornaments can also have non-sexual social functions, raising the possibility that observed sex differences in ornamentation are plastic. For example, females may invest in costly ornamentation more plastically, to protect body and reproductive ability in more adverse ecological conditions. We tested this hypothesis with experimental work on the mutually-ornamented common waxbill (Estrilda astrild), supplementing their diets either with pigmentary (lutein, a carotenoid) or non-pigmentary (vitamin E) antioxidants, or alleviating winter cold temperature. We found that both lutein and vitamin E supplementation increased red bill colour saturation in females, reaching the same mean saturation as males, which supports the hypothesis that female bill colour is more sensitive to environmental or physiological conditions. The effect of vitamin E, a non-pigment antioxidant, suggests that carotenoids were released from their antioxidant functions. Alleviating winter cold did not increase bill colour saturation in either sex, but increased the stability of female bill colour over time, suggesting that female investment in bill colour is sensitive to cold-mediated stress. Together, results show that waxbill bill sexual dichromatism is not stable. Instead, sexual dichromatism can be modulated, and even disappear completely, due to ecology-mediated plastic adjustments in female bill colour.

The evolution of sexually dimorphic traits in ecological gradients: an interplay between natural and sexual selection in hummingbirds

“…Given the evidence presented here and in other studies, sexual dimorphism can be seen as a product of pressures ranging from ecological differences between sexes [8,95] to differences as a result of intra- [7,9] and inter-sexual selection [74,96]. Although a universal trait that represents the strength of sexual selection can be convenient for comparative studies, it is likely that a single trait is insufficient, and that some traits useful as proxies in some clades are not in others [97].…”

Oestradiol reduces female bill colour in a mutually ornamented bird

“…In zebra finches, female bills that have redder hues contain more carotenoids, and bill sexual dichromatism is attributed to differences in concentration of red ketocarotenoids in bill tissue [70]. In both the common waxbill and the diamond firetail ( Stagonopleura guttata ), another mutually ornamented estrildid finch, red bills of females on a carotenoid-supplemented diet developed redder hues [14,71]. Together, these results suggest that E 2 -females may have reduced biotransformation and/or diverted carotenoids away from the bill to competing reproductive functions underlain by oestradiol, in line with hypotheses of carotenoid allocation trade-offs [72].…”

“…In the common waxbill, field data indicate that bill colour saturation is positively related to body condition in males, but not in females [83]. By contrast, female, but not male, waxbills were found to decrease bill colour saturation when their diet was poorer in carotenoids or antioxidants [14], and their bill colour saturation decreases or becomes unstable in colder weather [11,14]. These observations suggest that the potential signalling content of common waxbill bill colour differs between the sexes.…”

“…In sum, we found support for the hypothesis that reproductive physiology influences dynamic female investment in bill colour ornamentation, and that this process is at least partially mediated by oestradiol. To our knowledge, waxbill coloration is one of the very few documented examples of female-driven plastic sexual dichromatism due to changes in hormonal physiology (this study) or ecological conditions [11,14,45]. Other examples are the effect of melanocyte stimulating hormone on the darkness of a female-specific eye line in sand gobies ( Pomatoschistus minutus ) [84] and on the orange bellies of female two-spotted gobies ( Gobiusculus flavescens ) [85].…”

“…Previous work showed that waxbill beak sexual dichromatism is plastic and can disappear when both sexes are kept under the same favourable conditions in captivity [11,46]. Specifically, female, but not male, bill colour is sensitive to environmental conditions such as cold temperature and the availability of antioxidants (lutein and vitamin E) in the diet, which has led to the hypothesis that females plastically trade-off investment in ornamentation with maintaining optimal reproductive condition [11,14]. We housed mixed-sex groups of common waxbills and exposed half of the females to a continuous release of exogenous oestradiol (17β-estradiol) via subcutaneous implants, and during two months monitored changes in red bill colour of treated and control females, and of males.…”