Skewed performance distributions as evidence of motor constraint in sports and animal displays.

Animal displays (i.e. movement-based signals) often involve extreme behaviours that seem to push signallers to the limits of their abilities. If motor constraints limit display performance, signal evolution will be constrained, and displays can function as honest signals of quality. Existing approaches for measuring constraint, however, require multiple kinds of behavioural data. A method that requires only one kind could open up new research directions. We propose a conceptual model of performance under constraint, which predicts that the distribution of constrained performance will skew away from the constraint. We tested this prediction with sports data, because we know a priori that athletic performance is constrained and that athletes attempt to maximize performance. Performance consistently skewed in the predicted direction in a variety of sports. We then used statistical models based on the skew normal distribution to estimate the constraints on athletes and displaying animals while controlling for potential confounds and clustered data. We concluded that motor constraints tend to generate skewed behaviour and that skew normal models are useful tools to estimate constraints from a single axis of behavioural data. This study expands the toolkit for identifying, characterizing, and comparing performance constraints for applications in animal behaviour, physiology and sports.

Sex differences in song syntax and syllable diversity in testosterone-induced songs of adult male and female canaries.

BACKGROUND: Behavioral sex differences are widespread in the animal world. These differences can be qualitative (i.e., behavior present in one sex but not the other, a true sex dimorphism) or quantitative (behavior is present at a higher rate or quality in one sex compared to the other). Singing in oscine songbirds is associated with both types of differences. In canaries, female rarely sing spontaneously but they can be induced to do so by treatments with steroids. Song in these females is, however, not fully masculinized and exhibits relatively subtle differences in quality as compared with male song. We analyzed here sex differences in syllable content and syllable use between singing male and female canaries. METHODS: Songs were recorded from three groups of castrated male and three groups of photoregressed female canaries that had received Silastic™ implants filled with testosterone (T), with T plus estradiol (E2), or left empty (control). After 6 weeks of hormone treatment, 30 songs were recorded from each of the 47 subjects. Songs were segmented and each syllable was annotated. Various metrics of syllable diversity were extracted and network analysis was employed to characterize syllable sequences. RESULTS: Male and female songs were characterized by marked sex differences related to syllable use. Compared to females, males had a larger syllable-type repertoire and their songs contained more syllable types. Network analysis of syllable sequences showed that males follow more fixed patterns of syllable transitions than females. Both sexes, however, produced song of the same duration containing the same number of syllables produced at similar rates (numbers per second). CONCLUSIONS: Under the influence of T, canaries of both sexes are able to produce generally similar vocalizations that nevertheless differ in specific ways. The development of song during ontogeny appears to be a very sophisticated process that is presumably based on genetic and endocrine mechanisms but also on specific learning processes. These data highlight the importance of detailed behavioral analyses to identify the many dimensions of a behavior that can differ between males and females.

Male canaries normally sing complex songs at high rate while females only rarely sing very simple songs. Testosterone induces active singing in both male and female canaries, but female song is still not fully masculinized by these treatments even if song duration does not differ between the sexes. We analyzed the syllable repertoire and the sequence of use for different syllables in canaries of both sexes treated with testosterone or testosterone supplemented with estradiol. Compared to females, males had a larger syllable-type repertoire and their songs contained more syllable types. Syllable transitions were also more fixed in males. Sex differences in adult singing of canaries are thus a complex mixture of differences that result from the different endocrine condition of males and females (and are thus partially reversed by administration of exogenous testosterone) and of more stable differences that presumably develop during the ontogenetic process under the influence of endocrine and genetic differences and of differential learning processes. Canary song thus represents an outstanding model system to analyze the interaction between nature and nurture in the acquisition of a sophisticated learned behavior as well as the mechanisms controlling sex differences in vocal learning and production.

Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?

We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e., rapid repetitions of song elements. We analyzed >42,000 trills recorded over a period of 6 weeks from 3 groups of castrated males and 3 groups of photoregressed females that received Silastic™ implants filled with T, T plus estradiol or left empty as control. Effects of T on the number of trills, trill duration and percent of time spent trilling were all stronger in males than females. Irrespective of endocrine treatment, trill performance assessed by vocal deviations from the trill rate versus trill bandwidth trade-off was also higher in males than in females. Finally, inter-individual differences in syrinx mass were positively correlated with specific features of trills in males but not in females. Given that T increases syrinx mass and syrinx fiber diameter in males but not in females, these data indicate that sex differences in trilling behavior are related to sex differences in syrinx mass and syrinx muscle fiber diameter that cannot be fully suppressed by sex steroids in adulthood. Sexual differentiation of behavior thus reflects organization not only of the brain but also of peripheral structures.

Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?

We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e., rapid repetitions of song elements. We analyzed more than 42,000 trills recorded over a period of 6 weeks from 3 groups of castrated males and 3 groups of photoregressed females that received Silasticâ"¢ implants filled with T, T plus estradiol or left empty as control. Effects of T on the number of trills, trill duration and percent of time spent trilling were all stronger in males than females. Irrespective of endocrine treatment, trill performance assessed by vocal deviations from the trill rate versus trill bandwidth trade-off was also higher in males than in females. Finally, inter-individual differences in syrinx mass were positively correlated with trill production in males but not in females. Given that T increases syrinx mass and syrinx fiber diameter in males but not in females, these data indicate that sex differences in trilling behavior are related to sex differences in syrinx mass and syrinx muscle fiber diameter that cannot be fully reversed by sex steroids in adulthood. Sexual differentiation of behavior thus reflects organization not only of the brain but also of peripheral structures.

Testosterone treatment reveals marked sex differences in song diversity and syllable syntax in adult canaries.

Background. Behavioral sex differences are widespread in the animal world. These differences can be qualitative (i.e., behavior present in one sex but not the other, a true sex dimorphism) or quantitative (behavior is present at a higher rate or quality in one sex compared to the other). Singing in oscine songbirds is associated with both types of differences. In canaries, female rarely sing spontaneously but they can be induced to do so by treatments with steroids. Song in these females is however not fully masculinized and exhibits relatively subtle differences in quality as compared with male song. We analyzed here sex differences in syllable content and syllable use between singing male and female canaries. Methods. Songs were recorded from 3 groups of castrated male and 3 groups of photoregressed female canaries that had received Silasticâ"¢ implants filled with testosterone (T), with T plus estradiol (E2), or left empty (control). After 6 weeks of hormone treatment, 30 songs were recorded from each of the 47 subjects. Songs were segmented and each syllable was annotated. Various metrics of syllable diversity were extracted and network analysis was employed to characterize syllable sequences. Results. Male and female songs were characterized by marked sex differences related to syllable use. Compared to females, males had a larger syllable type repertoire and their songs contained more syllable types. Network analysis of syllable sequences showed that males follow more fixed patterns of syllable transitions than females. Both sexes however produced song of the same duration containing the same number of syllables produced at similar rates (numbers per second). Conclusions. Under the influence of T canaries of both sexes are able to produce generally similar vocalizations that nevertheless differ in specific ways. The development of song during ontogeny appears to be a very sophisticated process that is presumably based on genetic and endocrine mechanisms but also on specific learning processes. These data highlight the importance of detailed behavioral analyses in order to identify the many dimensions of a behavior that can differ between males and females.

Animal Culture: How a New Birdsong Went Viral.

A new white-throated sparrow song has overtaken most of Canada in less than 20 years. The explanation for this remarkably fast spread may lie in the southern migratory grounds, where populations from across Canada converge each winter.

Migration and the evolution of duetting in songbirds.

Many groups of animals defend shared resources with coordinated signals. The best-studied of these signals are the vocal duets produced by mated pairs of birds. Duets are believed to be more common among tropical-breeding species, but a comprehensive test of this hypothesis is lacking, and the mechanisms that generate latitudinal patterns in duetting are not known. We used a stratified sample of 372 songbird species to conduct the first broad-scale, phylogenetically explicit analysis of duet evolution. We found that duetting evolves in association with the absence of migration, but not with sexual monochromatism or tropical breeding. We conclude that the evolution of migration exerts a major influence on the evolution of duetting. The perceived association between tropical breeding and duetting may be a by-product of the migration-duetting relationship. Migration reduces the average duration of partnerships, potentially reducing the benefits of cooperative behaviour, including duetting. Ultimately, the evolution of coordinated resource-defence signals in songbirds may be driven by ecological conditions that favour sedentary lifestyles and social stability.

A locally funded Puerto Rican parrot (Amazona vittata) genome sequencing project increases avian data and advances young researcher education.

BACKGROUND: Amazona vittata is a critically endangered Puerto Rican endemic bird, the only surviving native parrot species in the United States territory, and the first parrot in the large Neotropical genus Amazona, to be studied on a genomic scale. FINDINGS: In a unique community-based funded project, DNA from an A. vittata female was sequenced using a HiSeq Illumina platform, resulting in a total of ~42.5 billion nucleotide bases. This provided approximately 26.89x average coverage depth at the completion of this funding phase. Filtering followed by assembly resulted in 259,423 contigs (N50 = 6,983 bp, longest = 75,003 bp), which was further scaffolded into 148,255 fragments (N50 = 19,470, longest = 206,462 bp). This provided ~76% coverage of the genome based on an estimated size of 1.58 Gb. The assembled scaffolds allowed basic genomic annotation and comparative analyses with other available avian whole-genome sequences. CONCLUSIONS: The current data represents the first genomic information from and work carried out with a unique source of funding. This analysis further provides a means for directed training of young researchers in genetic and bioinformatics analyses and will facilitate progress towards a full assembly and annotation of the Puerto Rican parrot genome. It also adds extensive genomic data to a new branch of the avian tree, making it useful for comparative analyses with other avian species. Ultimately, the knowledge acquired from these data will contribute to an improved understanding of the overall population health of this species and aid in ongoing and future conservation efforts.

Aggressiveness and size: a model and two tests.

Individual variation in aggressive behavior in animals might be caused by adaptive covariation with body size. We developed a model that predicts the benefits of aggressiveness as a function of body size. The model indicated that individuals of intermediate sizes would derive the greatest benefits from being aggressive. If we assume that the cost of aggression is approximately uniform with respect to body size, selection should favor higher aggression in intermediate-sized individuals than in large or small individuals. This prediction was tested by stimulating male Madagascar hissing cockroaches, Gromphadorhina portentosa, with disembodied antennae and recording the males' aggressive responses. Antennae from larger males evoked weaker responses in subjects, suggesting that males obtained information about their opponents' size from the opponents' antennae alone. After accounting for this effect, we found support for the key prediction of our model: aggressiveness peaked at intermediate sizes. Data from actual male-male interactions validated that the antenna assay accurately measured aggressiveness. Analysis of an independent data set generated by staging male-male interactions also supported the prediction that intermediate-sized males were most aggressive. We conclude that adaptive covariation between body size and aggressiveness explains some interindividual variation in aggressiveness.

Developmental environment affects risk-acceptance in the hissing cockroach, Gromphadorhina portentosa.

Consistent individual differences in the tendency to accept risk have been demonstrated in invertebrates, fish, birds, and mammals, including humans. These individual differences have been associated with size, growth rate, survival, and reproductive success. Little research, however, has investigated the effect of developmental environment on individual differences in risk-acceptance. Competing hypotheses offer different explanations of how variation in the quality of the developmental environment affects risk-acceptance in adults. The first hypothesis states that individuals developing in poor quality environments take risks because such behavior is their only means of obtaining adequate fitness returns. The second hypothesis states that individuals developing in poor environments avoid risk because their poor physical condition makes them especially vulnerable to injury or death. We measured several forms of risk-accepting behavior (exploration, foraging, and recovery after disturbance) in male hissing cockroaches (Gromphadorhina portentosa) that had developed in nutritional and social environments of varying quality. Individuals raised on poor nutrition diets exhibited lower levels of risk-acceptance than those raised on high nutrition diets. Risk-acceptance among individuals that developed on poor nutrition diets was negatively correlated with body size. We conclude that quality of developmental environment affects risk-acceptance across behavioral contexts in male hissing cockroaches. Our findings are consistent with the hypothesis that condition-dependent vulnerability mediates the relationship between developmental environment and risk-acceptance.

Constrained performance in a communication network: implications for the function of song-type matching and for the evolution of multiple ornaments.

Many species of territorial songbirds exhibit a behavior known as song-type matching, in which a male sings the same song type that his neighbor is singing. Song-type matching is associated with increased aggression, but researchers have not come to a consensus on its adaptive function. Building on studies that identify singing performance as a variable relevant to sexual selection, we hypothesize that higher-performance singers benefit from matching their opponent's song type because matching improves eavesdroppers' ability to compare the two males' performances. We present a model of song-type choice that predicts that males that can outperform their rivals benefit by matching. In contrast, lower-performance males should avoid both matching and being matched. Our hypothesis is compatible with some existing hypotheses of song-matching function, but it is not compatible with the hypothesis that song matching is a conventional signal of aggression. We offer unique predictions that could be used to test our idea. We speculate that lower-performance individuals might have driven the evolution of repertoire complexity because they stand to benefit from novel, unmatchable songs. The phenomenon that dissimilar signals are less accurately compared than similar signals may favor the evolution of multiple ornaments and of plastic signal development (e.g., song learning) in general.

Duetting in space: a radio-telemetry study of the black-bellied wren.

In many birds, individuals 'answer' the songs of their pair-mates to produce vocal 'duets'. One hypothesized function of song answering is that it prevents extra-pair birds from intruding into the duetting pair's territory to obtain copulations or usurp one of the pair-mates. In this capacity, answering may signal that the pair-mates are close together, and so are prepared to defend against such an intrusion. Another functional hypothesis states that answering helps pair-mates maintain contact, and so predicts that a bird is more likely to approach its mate after a duet than after a solo song. I used radio-telemetry to monitor the distance between mated black-bellied wrens (Pheugopedius fasciatoventris). I found that birds of both sexes were more likely to answer their mate's song when the mate was close, and that maximum duet length was negatively related to the distance between pair-mates. Furthermore, song answering positively affected the likelihood of one pair-mate approaching the other after a song. In a significant majority of the approaches after duet songs, the answering bird approached the initiator. I conclude that in the black-bellied wren, (i) the occurrence and duration of vocal duets covary with physical closeness and (ii) contact maintenance is a secondary function of duet participation.