Oestradiol reduces female bill colour in a mutually ornamented bird.

Carotenoid-based colour signals can be costly to produce and maintain, and trade-offs between signalling and other fitness traits are expected. In mutually ornamented species, trade-offs with reproduction may be stronger for females than males, because females often dedicate more resources to offspring production, which may lead to plastic investment in colour signals and plastic sexual dichromatism. Oestradiol is a candidate mediator of this trade-off because it regulates reproductive physiology and may also influence the expression of coloration. We tested this hypothesis by giving female common waxbills (Estrilda astrild) either oestradiol (17ß-oestradiol) or empty implants during the early breeding season and measured spectral reflectance of carotenoid-based bill coloration weekly for two months. Using a model of avian vision, we found that bill colour in oestradiol-implanted females became less saturated, less red in hue and brighter, compared with control females and with unimplanted males. This resulted in a change in bill sexual dichromatism from imperceptible to perceptible. Results support the hypothesis that female reproductive physiology influences investment in coloration through changes in oestradiol and show a form of female-driven plastic sexual dichromatism. Greater sensitivity of female colour to physiological and/or environmental conditions helps explain why differences in sexual dichromatism among species differing in ecology often evolve owing to changes in female rather than male phenotype.

A test of context- and sex-dependent dopaminergic effects on the behavior of a gregarious bird, the common waxbill, Estrilda astrild.

The dopaminergic (DAergic) system has well-known influences on behavioral and cognitive functions. Previous work with common waxbills (Estrilda astrild) reported context-specific DAergic effects that could have been due to social environment. Manipulating the dopamine D2-like receptor family (D2R) pathways had opposing effects on behavior depending on whether waxbills were tested alone or in a small cage with a mirror as a social stimulus. As waxbills are highly gregarious, it was hypothesized that being alone or perceiving that they have a companion might explain this context dependence. To test context-dependent DAergic effects, we compared behavioral effects of D2R manipulation in waxbills in the same familiar environment, but either alone or with a familiar, same-sex companion. We found that D2R agonism decreased movement and feeding, similar to previous results when testing waxbills alone. However, contrary to the hypothesis of dependence on social context, we found that the behavioral effects of the D2R agonist were unchanged when waxbills were tested with a companion. The context dependence reported earlier might thus be due to other factors, such as the stress of being in a novel environment (small cage) or with an unfamiliar social stimulus (mirror image). In tests with a companion, we also found a sex-specific social effect of D2R manipulation: D2R blocking tended to decrease aggression in males but to increase it in females. Together with past work, our results suggest that DAergic effects on behavior involve different types of context or sex dependence.

Experimental evidence for a role of dopamine in avian personality traits.

There is increasing interest in the genetic and physiological bases of behavioural differences among individuals, namely animal personality. One particular dopamine (DA) receptor gene (the dopamine receptor D4 gene) has been used as candidate gene to explain personality differences, but with mixed results. Here, we used an alternative approach, exogenously manipulating the dopaminergic system and testing for effects on personality assays in a social bird species, the common waxbill (Estrilda astrild). We treated birds with agonists and antagonists for DA receptors of both D1 and D2 receptor pathways (the latter includes the D4 receptor) and found that short-term manipulation of DA signalling had an immediate effect on personality-related behaviours. In an assay of social responses (mirror test), manipulation of D2 receptor pathways reduced time spent looking at the social stimulus (mirror image). Blocking D2 receptors reduced motor activity in this social assay, while treatment with a D2 receptor agonist augmented activity in this social assay but reduced activity in a non-social behavioural assay. Also, in the non-social assay, treatment with the D1 receptor antagonist markedly increased time spent at the feeder. These results show distinct and context-specific effects of the dopaminergic pathways on waxbill personality traits. Our results also suggest that experimental manipulation of DA signalling can disrupt a behavioural correlation (more active individuals being less attentive to mirror image) that is habitually observed as part of a behavioural syndrome in waxbills. We discuss our results in the context of animal personality, and the role of the DA system in reward and social behaviour.

Effects of mesotocin manipulation on the behavior of male and female common waxbills.

The oxytocin family of neuropeptides is implicated in the regulation of sociality across vertebrates. Non-mammalian homologs of oxytocin, such as isotocin in fish and mesotocin in amphibians, reptiles and birds, all play crucial roles modulating social and reproductive behavior. In this study, we exogenously manipulated the mesotocinergic system in a highly social bird, the common waxbill Estrild astrild, and tested the effects on affiliative and aggressive behavior by performing tests of competition over food. Birds treated with mesotocin decreased almost all the behaviors we studied (movement, feeding, allopreening), while birds treated with an oxytocin antagonist showed a reduction only in social behaviors (aggressions and allopreening). We also found two sex-specific effects: mesotocin reduced allopreening more in males than females, and the oxytocin antagonist reduced aggressiveness only in females. Our results suggest sex-specific effects in the modulation of affiliative and aggressive behaviors via mesotocinergic pathways.

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

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.

Cleaner blues: Condition-dependent colour and cleaner fish service quality.

While vivid colours in sexual signals can provide information on individual quality, vivid colours in interspecific signals have been interpreted mostly as indicating species identity and maximizing signal detection. Here we investigate if colour differences in an interspecific signal could also indicate relevant aspects of individual quality because, similarly to sexual signalling, in interspecific communication it could sometimes be advantageous to assess individual quality. For example when interacting with cleaner species, clients should benefit from assessing which individual cleaners provide better service. Since oxidative stress commonly influence condition-dependent colour signals, we oxidized the diet of cleaner wrasses (Labroides dimidiatus) in laboratory conditions to test if this affects their vivid blue skin colour and the quality of their cleaning service. Compared to controls, experimental cleaners decreased blue colour saturation after the oxidized diet treatment, decreased the quality of their cleaning service by performing less tactile stimulation and, although clients in the laboratory were de-parasitized, also tended to decrease the touching the client with the mouth. We used visual modelling, based on the spectral sensitivity of vision in various client species, to show that some client species can perceive these changes in cleaner blue colour saturation, while other client species not. We suggest that, similarly to sexual signals, some vivid colours used in interspecific communication may convey information on aspects of individual quality that are relevant to heterospecifics.

A genetic mechanism for sexual dichromatism in birds.

Sexual dichromatism, a difference in coloration between males and females, may be due to sexual selection for ornamentation and mate choice. Here, we show that carotenoid-based dichromatism in mosaic canaries, a hybrid phenotype that arises in offspring of the sexually dichromatic red siskin and monochromatic canaries, is controlled by the gene that encodes the carotenoid-cleaving enzyme ß-carotene oxygenase 2 (BCO2). Dichromatism in mosaic canaries is explained by differential carotenoid degradation in the integument, rather than sex-specific variation in physiological functions such as pigment uptake or transport. Transcriptome analyses suggest that carotenoid degradation in the integument might be a common mechanism contributing to sexual dichromatism across finches. These results suggest that differences in ornamental coloration between sexes can evolve through simple molecular mechanisms controlled by genes of major effect.