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.

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.

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.

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.

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.

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.

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.

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.

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.

Urban birdsongs: higher minimum song frequency of an urban colonist persists in a common garden experiment.

Environmental changes caused by urbanization and noise pollution can have profound effects on acoustic communication. Many organisms use higher sound frequencies in urban environments with low-frequency noise, but the developmental and evolutionary mechanisms underlying these shifts are generally unknown. We used a common garden experiment to ask whether changes in minimum song frequency observed 30 years after a songbird colonized an urban environment are a consequence of behavioural flexibility. We captured male juvenile dark-eyed juncos, Junco hyemalis thurberi, from two populations (urban and mountain) soon after they reached independence (aged 25-40 days), raised them in identical indoor aviaries and studied their songs at an age of 3 years. We found that the large population difference in minimum frequency observed in the field persisted undiminished in the common garden despite the absence of noise. We also found some song sharing between the common garden and natal field populations, indicating that early song memorization before capture could contribute to the persistent song differences in adulthood. These results are the first to show that frequency shifts in urban birdsong are maintained in the absence of noise by genetic evolution and/or early life experiences.

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.

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.

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.

Choice of high-quality mates versus avoidance of low-quality mates.

Research in sexual selection assumes that individuals attempt to choose high-quality mates, and that sexual signals evolve to indicate high quality. But it may often be more important to instead discriminate and avoid low-quality mates, thus reducing the likelihood of large penalties in fitness. We show, using simulations, that avoidance of low-quality mates (i.e., rejecting low-quality and accepting either high- or medium-quality mates) evolves in socio-ecological circumstances such as monogamy with moderate opportunities for choice, costly choice, or abundant low-quality mates. We also show that this strategy is qualitatively different from choosing high-quality mates (i.e., preferring high-quality over medium- and low-quality mates). Rather than selecting signals that distinguish high- from low- and medium-quality mates, avoiding low-quality mates selects for signals or cues attuned at discriminating low-quality mates from the remaining (e.g., low-cost signals, absence of signaling mistakes). This may help explain the high diversity of sexual signals in nature, and their high evolutionary turnover with frequent losses and replacements (rather than reductions/increases of the same signal) over evolutionary time.

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.

The comparative evidence for urban species sorting by anthropogenic noise.

Anthropogenic noise is more intense at lower sound frequencies, which could decrease urban tolerance of animals with low-frequency vocalizations. Four large comparative studies tested whether anthropogenic noise filters bird species according to the sound frequencies they use and produced discrepant results. We reanalysed data from these studies to explain their different results. Urban tolerance of bird species (defined here as often occurring and breeding in cities) is very weakly related to urban preference or relative abundance (defined based on changes in population density from urban to nearby rural environments). Data on urban preference/abundance are potentially accurate for individual cities but differ among cities for the same species, whereas existing data on urban tolerance are coarser but provide a more global synthesis. Cross-species comparisons find a positive association between the sound frequency of song and urban tolerance, but not urban preference/abundance. We found that showing an association between song frequency and urban tolerance requires controlling for additional species traits that influence urban living. On the contrary, controlling for other species traits is not required to show a positive association between song frequency and use of noisy relative to quiet areas within the same type of environment. Together, comparative evidence indicates that masking by urban noise is part of a larger set of factors influencing urban living: all else being equal, species with high-frequency sounds are more likely to tolerate cities than species with low-frequency sounds, but they are not more likely to prefer, or to be more abundant in, urban than non-urban habitats.

Speciation is associated with changing ornamentation rather than stronger sexual selection.

Although sexual ornamentation mediates reproductive isolation, comparative evidence does not support the hypothesis that stronger sexual selection promotes speciation. Prior analyses have neglected the possibility that decreases in ornamentation may also promote speciation, such that both increases and decreases in the strength of sexual selection and associated changes in ornamentation promote speciation. To test this hypothesis, we studied color ornamentation in one of the largest and fastest avian radiations, the estrildid finches. We show that more ornamented lineages do not speciate more, even though they tend to have faster rates of ornamental evolution, whereas changes in ornamentation (i.e., increases or decreases) are associated with speciation. This indicates that divergence in sexually selected ornamentation, rather than stronger sexual selection, promotes or is otherwise associated with speciation. We also show that gregariousness and investment in reproduction are related to the elaboration of some ornamental traits, suggesting ecological influences on speciation mediated by ornamentation. We conclude that past work focusing specifically on the strength of sexual selection may have greatly underestimated the importance of sexual ornamentation for speciation.

Shared songs are of lower performance in the dark-eyed junco.

Social learning enables the adjustment of behaviour to complex social and ecological tasks, and underlies cultural traditions. Understanding when animals use social learning versus other forms of behavioural development can help explain the dynamics of animal culture. The dark-eyed junco (Junco hyemalis) is a songbird with weak cultural song traditions because, in addition to learning songs socially, male juncos also invent or improvise novel songs. We compared songs shared by multiple males (i.e. socially learned) with songs recorded from only one male in the population (many of which should be novel) to gain insight into the advantages of social learning versus invention or improvisation. Song types shared by multiple males were on average of lower performance, on aspects of vocal performance that have been implicated in agonistic communication in several species. This was not explained by cultural selection among socially learned songs (e.g. selective learning) because, for shared song types, song performance did not predict how many males shared them. We discuss why social learning does not maximize song performance in juncos, and suggest that some songbirds may add novel songs to culturally inherited repertoires as a means to acquire higher-quality signals.

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.