Bullying as an advertisement of social dominance in common waxbills.

Bullying consists of preferentially attacking individuals lowest in the dominance hierarchy, and its functions are unclear because the most subordinate individuals do not pose social challenges to the aggressor. Instead, conflict is expected mostly between individuals of similar dominance rank or socially distant (i.e. weakly associated), among whom dominance relationships may not be well established. A possible function of bullying is that it may be used as a low-risk strategy of showing-off dominance to relevant third parties. To study this hypothesis, we monitored aggressions during feeding, the composition of audiences, dominance hierarchy and social network of common waxbills (Estrilda astrild) in an open-air mesocosm, and tested (i) whether their aggressions show a pattern of bullying, and (ii) whether audience effects influence aggressiveness. Waxbills showed bullying, most often attacking the lowest ranking individuals rather than socially distant individuals or those of similar dominance rank, and aggressions increased when the audience included socially distant individuals, indicating a signalling function of bullying. Showing-off dominance in the presence of socially distant individuals may be a strategy to manage dominance hierarchies, avoiding direct fights with potentially dangerous opponents in the audience. We suggest that bullying is a safe manner of managing dominance hierarchies, by signalling dominance status to potential opponents.

Same Colors for Different Functions: Implications for the Evolution of Carotenoid-Based Ornamentation.

AbstractSexual ornamentation is often assumed to be costly, allowing honest signaling of individual quality, and carotenoid-based colors have been proposed to bear significant costs. If carotenoid-based colors are costly to produce, sexually selected signals should use more concentrated carotenoid pigments and have more saturated color than nonsexual signals, where honesty-guaranteeing costs are not required. We tested this prediction comparing carotenoid-based colors across canaries, goldfinches, and allies because many of these species use yellow plumage as sexual ornamentation but also have yellow rumps that appear to be nonsexual flash marks. Only in the breast, but not the rump, was there an asymmetric codistribution of male and female color saturation, with males similarly or more saturated than females, indicating evolution of breast color by sexual selection. Yellow was not consistently more saturated in the breast than in the rump, and the codistribution of rump and breast color saturation indicated that saturated rumps can persist irrespective of breast color. This challenges the assumption that carotenoid-based colors bear significant costs. The use of carotenoid coloration as sexual signals in this clade may instead be due to social costs, cost-free index mechanisms for signaling quality, and/or socially monogamous species evolving low-cost signals to mostly discriminate against the lowest-quality mates.

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.

Body size and sexual selection shaped the evolution of parrot calls.

Morphology, habitat and various selective pressures (e.g. social and sexual selection) can influence the evolution of acoustic signals, but the relative importance of their effects is not well understood. The order Psittaciformes (parrots, sensu lato) is a large clade of very vocal and often gregarious species for which large-scale comparative studies of vocalizations are lacking. We measured acoustic traits (duration, sound frequency, frequency bandwidth and sound entropy) of the predominant call type for >200 parrot species to test: (1) for associations with body size; (2) the acoustic adaptation hypothesis (AAH) (predicting differences between forest and open-habitat species); (3) the social complexity hypothesis (predicting more complex calls in gregarious species) and (4) influences of sexual selection (predicting correlated evolution with colour ornamentation). Larger species had on average longer calls, lower sound frequency and wider frequency bandwidth. These associations with body size are all predicted by physical principles of sound production. We found no evidence for the acoustic adaptation and social complexity hypotheses, but perhaps social complexity is associated with vocal traits not studied here, such as call repertoire sizes. More sexually dichromatic species had on average simpler calls (shorter, with lower entropy and narrower frequency bandwidth) indicating an influence of sexual selection, namely an evolutionary negative correlation between colour ornamentation and elaborate acoustic signals, as predicted by the transference hypothesis. Our study is the first large-scale attempt at understanding acoustic diversity across the Psittaciformes, and indicates that body size and sexual selection influenced the evolution of species differences in vocal signals.

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.

The Allometry of Sound Frequency Bandwidth in Songbirds.

AbstractTheory predicts that allometric constraints on sound production should be stronger for the lower frequencies of vocalizations than for the higher frequencies, which could originate from an allometry for sound frequency bandwidth. Using song recordings of approximately 1,000 passerine species (from >75% passerine genera), we show a significantly steeper allometry for the lower song frequencies than for the higher song frequencies, resulting in a positive allometry of frequency bandwidth: larger species can use wider bandwidths than smaller species. The bandwidth allometry exists in songbirds (oscines) but not in nonoscine passerines, indicating that it emerges from a combination of constraints to sound frequency production or transmission and the evolved behavior of oscines: unlike the narrow bandwidths of most nonoscine songs, the learned songs of oscines often use wide bandwidths that can be limited by both lower and upper constraints to sound frequency. This bandwidth allometry has implications for several research topics in acoustic communication.

The lag-time constraint for behavioural plasticity.

Environmental instability (i.e. environments changing often) can select fixed phenotypes because of the lag time of plastically adapting to environmental changes, known as the lag-time constraint. Because behaviour can change rapidly (e.g. switching between foraging strategies), the lag-time constraint is not considered important for behavioural plasticity. Instead, it is often argued that responsive behaviour (i.e. behaviour that changes according to the environment) evolves to cope with unstable environments. But proficiently performing certain behaviours may require time for learning, for practising or, in social animals, for the group to adjust to one's behaviour. Conversely, not using certain behaviours for a period of time can reduce their level of performance. Here, using individual-based evolutionary simulations, we show that environmental instability selects for fixed behaviour when the ratio between the rates of increase and reduction in behavioural performance is below a certain threshold; only above this threshold does responsive behaviour evolve in unstable environments. Thus, the lag-time constraint can apply to behaviours that attain high performance either slowly or rapidly, depending on the relative rate with which their performance decreases when not used. We discuss these results in the context of the evolution of reduced behavioural plasticity, as seen in fixed personality differences.

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.

Haemosporidian parasites missed the boat during the introduction of common waxbills (Estrilda astrild) in Iberia.

Exotic species can experience fast expansion in new environments, especially if they left their pathogens behind (Enemy Release hypothesis) or brought novel pathogens to the native competitors (Novel Weapon hypothesis). Common waxbills (Estrilda astrild) are native to sub-Saharan Africa and invaded west Iberia since the 1960s. Past haemosporidian parasite surveys at four locations in Portugal showed that waxbills can be infected with parasites, though with very low prevalence. However, it is not known if this pattern generalizes across their distribution range, or if there are geographic differences in parasite prevalence. It is also not discussed if this is a case of Enemy Release, as opposed to waxbills being also little parasitized in their native range. We screened 617 waxbills in 23 sites in Portugal and detected nine parasite lineages, most of them only known to the Palearctic. Only ten individuals were parasitized, and there was no significant geographical pattern on the prevalence. Overall, this population shows very low prevalence of haemosporidians (1.6% prevalence), which contrasts with significantly higher prevalence in native grounds, as compiled from the literature. These data support Enemy Release as the most likely hypothesis, which may have been important for their success as an exotic species.

Communication Value of Mistakes in Dark-Eyed Junco Song.

Sexual signals contain information on individual quality or motivation, and most explanations for their reliability are based on signal costs. A recent suggestion is that signaling mistakes, defined as deviations from typical signal design, provide cues on individual quality, contributing to reliable communication even when signal design is not costly. We describe several atypical song traits in dark-eyed juncos (Junco hyemalis) that may be mistakes during song production or development and occur in up to 6% of songs. These putative mistakes were more frequent in an urban versus a wildland population, and individuals differed in their frequency of mistakes. Some atypical signals were more frequent in younger males or were negatively related to paternity success, supporting the hypothesis that fewer mistakes indicate individual quality. We also discuss unexpected results, such as some atypical signals being more frequent in more ornamented males and in songs with lower performance demands. Song consistency (similarity across syllable renditions) was positively related to male age and paternity success; nonetheless, relations with paternity were stronger when looking at the most deviant syllable renditions, suggesting that the perceptual salience of large mistakes may mediate receiver responses to song consistency. Results indicate that signaling mistakes reveal relevant information to play a role in communication.

Studying the silent side of birdsong.

The quality of complex communication signals, such as birdsong, is difficult to assess and compare across individuals or species. A new study on skylark song avoids the problem of signal complexity by assessing motor performance during the silent gaps of songs. This provides a metric of song quality applicable to species with very diverse songs, which facilitates novel types of analyses and comparisons in avian bioacoustics.

Hormonal, behavioral, and life-history traits exhibit correlated shifts in relation to population establishment in a novel environment.

Climate change, habitat alteration, range expansions, and biological invasions are all predicted to require rapid shifts in multiple traits including behavior and life history, both for initial population establishment and subsequent adaptation. Hormonal mechanisms likely play a key role in facilitating or constraining plastic and genetic responses for suites of traits, but few studies have evaluated their role in shaping contemporary adaptation or diversification. We examined multiple phenotypic adjustments and associated hormonal changes following a recent (early 1980s) colonization event, in which a temperate-breeding songbird, the dark-eyed junco (Junco hyemalis), became established in the Mediterranean climate of San Diego, California. The milder climate has led to an extended breeding season and year-round residency, and we document shifts in multiple sexually selected behaviors and plumage traits. Testosterone titers in San Diego were elevated for longer but with a lower peak value compared to a nearby native-range population, and correlations between testosterone and related traits were similar within and among populations. A common garden study indicated that changes in testosterone likely represent plastic responses to the less seasonal environment of the city, providing the context against which subsequent genetic changes in morphology likely occurred. We argue that correlated shifts in multiple traits, organized by underlying physiology, may be a generally important element of many successful adjustments to changing environments.

Nesting and acoustic ecology, but not phylogeny, influence passerine urban tolerance.

Urbanization is one of the most extensive and ecologically significant changes happening to terrestrial environments, as it strongly affects the distribution of biodiversity. It is well established that native species richness is reduced in urban and suburban areas, but the species traits that predict tolerance to urbanization are yet little understood. In birds, one of the most studied groups in this respect, evidence is appearing that acoustic traits influence urban living, but it remains unknown how this compares to the effects of more obvious ecological traits that facilitate urban living. Therefore, it remains unclear whether acoustic communication is an important predictor of urban tolerance among species. Here, with a comparative study across 140 European and North American passerines, I show that high song frequency, which is less masked by the low-frequency anthropogenic noise, is associated with urban tolerance, with an effect size over half that of the most important ecological trait studied: off-ground nesting. Other nesting and foraging traits accepted to facilitate urban living did not differ for species occurring in urban environments. Thus, the contribution of acoustic traits for passerine urban tolerance approximates that of more obvious ecological traits. Nonetheless, effect sizes of the biological predictors of urban tolerance were low and the phylogenetic signal for urban tolerance was null, both of which suggest that factors other than phenotypic traits have major effects on urban tolerance. A simple possibility is exposure to urbanization, as there was a higher proportion of urban-tolerant species in Europe, which is more urbanized than North America.

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.

Birdsong performance and the evolution of simple (rather than elaborate) sexual signals.

Sexual signals are often elaborate as a result of sexual selection for signals of individual quality. Contrary to expectation, however, the elaboration of signals such as birdsong is not related to the strength of sexual selection across species. With a comparative study across wood warblers (family Parulidae), we show a compromise between advertising the performance of trills (syllable repetitions) and song complexity, which can result in the evolution of simple, rather than elaborate, song. Species with higher trill performance evolved simple songs with more extensive trilled syntax. This advertises trill performance but reduces syllable diversity in songs. These two traits are commonly sexually selected in songbirds, but indexes of sexual selection were not related to either in wood warblers. This is consistent with sexual selection targeting different traits in different species, sometimes resulting in simple signals. We conclude that the evolution of sexual signals can be unpredictable when their physiology affords multiple or, as here, opposing ways of advertising individual quality.

Contingency and determinism in the evolution of bird song sound frequency.

Sexual signals are archetypes of contingent evolution: hyper-diverse across species, often evolving fast and in unpredictable directions. It is unclear to which extent their evolutionary unpredictability weakens deterministic evolution, or takes place bounded by deterministic patterns of trait evolution. We compared the evolution of sound frequency in sexual signals (advertisement songs) and non-sexual social signals (calls) across > 500 genera of the crown songbird families. Contrary to the acoustic adaptation hypothesis, we found no evidence that forest species used lower sound frequencies in songs or calls. Consistent with contingent evolution in song, we found lower phylogenetic signal for the sound frequency of songs than calls, which suggests faster and less predictable evolution, and found unpredictable direction of evolution in lineages with longer songs, which presumably experience stronger sexual selection on song. Nonetheless, the most important deterministic pattern of sound frequency evolution-its negative association with body size-was stronger in songs than calls. This can be explained by songs being longer-range signals than most calls, and thus using sound frequencies that animals of a given size produce best at high amplitude. Results indicate that sexual selection can increase aspects of evolutionary contingency while strengthening, rather than weakening, deterministic patterns of evolution.

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.

Evolution of female carotenoid coloration by sexual constraint in Carduelis finches.

BACKGROUND: Females often express the same ornaments as males to a similar or lesser degree. Female ornaments can be adaptive, but little is known regarding their origins and mode of evolution. Current utility does not imply evolutionary causation, and therefore it is possible that female ornamentation evolved due to selection on females, as a correlated response to selection on males (sexual constraint), or a combination of both. We tested these ideas simulating simple models for the evolution of male and female correlated traits, and compared their predictions against the coloration of finches in the genus Carduelis. RESULTS: For carotenoid-based ornamental coloration, a model of sexual constraint on females fits the Carduelis data well. The two alternative models (sexual constraint on males, and mutual constraint) were rejected as causing the similarities in carotenoid coloration between males and females. For melanin coloration, the correlation between the sexes was weaker, indicating that males and females evolved independently to a greater extent. CONCLUSIONS: This indicates that sexual constraint on females was an important mechanism for the evolution of ornamental carotenoid coloration in females, but less so for melanin coloration. This does not mean that female carotenoid coloration is non-adaptive or maladaptive, because sexual dichromatism could evolve if it were maladaptive. It suggests, however, that most evolution of female carotenoid coloration was male-driven and, when adaptive, may not be an adaptation stricto sensu.

Independent evolution of song diversity and song motor performance in canaries, goldfinches and allies indicates clade-specific trade-offs in birdsong.

The diversity and the motor performance of birdsongs can both be sexually selected. In wood warblers, most species with high motor performance sing a greater proportion of trills, presumably to advertise performance, and thus have lower syllable diversity. We tested if this trade-off between motor performance and syllable diversity extends to canaries, goldfinches and allies, a clade with much longer and more varied songs. We assembled a molecular phylogeny and inferred song motor performance based on the speed of frequency modulation either in trills or in within-song intervals. The two metrics of performance were positively, but only mildly, related across species. While performance evaluated in intervals had high phylogenetic signal, performance evaluated in trills changed independently of phylogeny and was constrained by body size. Species in densely vegetated habitats sang fewer trills, but did not differ in motor performance. Contrary to wood warblers, song motor performance did not predict the proportion of trilled syllables nor within-song syllable diversity, perhaps because large differences in the song duration of canaries, goldfinches and allies prevent trills from severely compromising syllable diversity. Opposed results in wood warblers and in these finches indicate the existence of clade-specific trade-offs in the evolution of birdsong.

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.