The effect of environmental variation on the relationship between survival and risk-taking behaviour in a migratory songbird.

Temporal changes in environmental conditions may play a major role in the year-to-year variation in fitness consequences of behaviours. Identifying environmental drivers of such variation is crucial to understand the evolutionary trajectories of behaviours in natural contexts. However, our understanding of how environmental variation influences behaviours in the wild remains limited. Using data collected over 14 breeding seasons from a collared flycatcher (Ficedula albicollis) population, we examined the effect of environmental variation on the relationship between survival and risk-taking behaviour, a highly variable behavioural trait with great evolutionary and ecological significance. Specifically, using annual recapture probability as a proxy of survival, we evaluated the specific effect of predation pressure, food availability, and mean temperature on the relationship between annual recapture probability and risk-taking behaviour (measured as flight initiation distance [FID]). We found a negative trend, as the relationship between annual recapture probability and FID decreased over the study years and changed from positive to negative. Specifically, in the early years of the study, risk-avoiding individuals exhibited a higher annual recapture probability, whereas in the later years, risk-avoiders had a lower annual recapture probability. However, we did not find evidence that any of the considered environmental factors mediated the variation in the relationship between survival and risk-taking behaviour.

Responses in the breeding parameters of the collared flycatcher to the changing climate.

Global climate change involves various aspects of climate, including precipitation changes and declining surface wind speeds, but studies investigating biological responses have often focused on the impacts of rising temperatures. Additionally, related long-term studies on bird reproduction tend to concentrate on breeding onset, even though other aspects of breeding could also be sensitive to the diverse weather aspects. This study aimed to explore how multiple aspects of breeding (breeding onset, hatching delay, breeding season length, clutch size, fledgling number) were associated with different weather components. We used an almost four-decade-long dataset to investigate the various aspects of breeding parameters of a collared flycatcher (Ficedula albicollis) population in the Carpathian Basin. Analyses revealed some considerable associations, for example, breeding seasons lengthened with the amount of daily precipitation, and clutch size increased with the number of cool days. Parallel and opposing changes in the correlated pairs of breeding and weather parameters were also observed. The phenological mismatch between prey availability and breeding time slightly increased, and fledgling number strongly decreased with increasing mistiming. Our results highlighted the intricate interplay between climate change and the reproductive patterns of migratory birds, emphasizing the need for a holistic approach. The results also underscored the potential threats posed by climate change to bird populations and the importance of adaptive responses to changing environmental conditions.

Are brood sex ratios adaptive?-The effect of experimentally altered brood sex ratio on nestling growth, mortality and recruitment.

Brood sex ratios (BSRs) have often been found to be nonrandom in respect of parental and environmental quality, and many hypotheses suggest that nonrandom sex ratios can be adaptive. To specifically test the adaptive value of biased BSRs, it is crucial to disentangle the consequences of BSR and maternal effects. In multiparous species, this requires cross-fostering experiments where foster parents rear offspring originating from multiple broods, and where the interactive effect of original and manipulated BSR on fitness components is tested. To our knowledge, our study on collared flycatchers (Ficedula albicollis) is the first that meets these requirements. In this species, where BSRs had previously been shown to be related to parental characteristics, we altered the original BSR of the parents shortly after hatching by cross-fostering nestlings among trios of broods and examined the effects on growth, mortality and recruitment of the nestlings. We found that original and experimental BSR, as well as the interaction of the two, were unrelated to the fitness components considered. Nestling growth was related only to background variables, namely brood size and hatching rank. Nestling mortality was related only to hatching asynchrony. Our results therefore do not support that the observed BSRs are adaptive in our study population. However, we cannot exclude the possibility of direct effects of experimentally altered BSRs on parental fitness, which should be evaluated in the future. In addition, studies similar to ours are required on various species to get a clearer picture of the adaptive value of nonrandom BSRs.

Functional Integration of Multiple Sexual Ornaments: Signal Coherence and Sexual Selection.

AbstractThe sexual ornamentation of animals typically consists of multiple distinct traits. The classical research approach focuses on differences among these traits, but this approach may often be misleading because of correlations among distinct sexual traits of similar origins. There are many published studies on the correlation structures of sexual traits, but the way receivers take into account the components of an integrated, multicomponent trait system remains mostly unknown. Here, we propose a general analytical framework to assess the possible sexual selection consequences of within-individual coherence in the expression of multiple correlated sexual traits. We then apply this framework to a long-term mutual plumage coloration data set from a wild bird population. The results suggest that the coherence of component plumage color traits is not sexually selected. However, component trait coherence affects sexual selection on integrated plumage color. When assessing across-spectrum plumage reflectance, receivers choosing mates apparently disregard a component trait if it is inconsistent with the overall expression of other components. This indicates that separately examining and manipulating distinct sexual traits may often be misleading. Theoretical and empirical studies should further explore the effects of coherence on the ornament-preference coevolution.

Individual differences in song plasticity in response to social stimuli and singing position.

Individual animals can react to the changes in their environment by exhibiting behaviors in an individual-specific way leading to individual differences in phenotypic plasticity. However, the effect of multiple environmental factors on multiple traits is rarely tested. Such a complex approach is necessary to assess the generality of plasticity and to understand how among-individual differences in the ability to adapt to changing environments evolve. This study examined whether individuals adjust different song traits to varying environmental conditions in the collared flycatcher (Ficedula albicollis), a passerine with complex song. We also aimed to reveal among-individual differences in behavioral responses by testing whether individual differences in plasticity were repeatable. The presence of general plasticity across traits and/or contexts was also tested. To assess plasticity, we documented (1) short-scale temporal changes in song traits in different social contexts (after exposition to male stimulus, female stimulus or without stimuli), and (2) changes concerning the height from where the bird sang (singing position), used as a proxy of predation risk and acoustic transmission conditions. We found population-level relationships between singing position and both song length (SL) and complexity, as well as social context-dependent temporal changes in SL and maximum frequency (MF). We found among-individual differences in plasticity of SL and MF along both the temporal and positional gradients. These among-individual differences in plasticity were repeatable. Some of the plastic responses correlated across different song traits and environmental gradients. Overall, our results show that the plasticity of bird song (1) depends on the social context, (2) exists along different environmental gradients, and (3) there is evidence for trade-offs between the responses of different traits to different environmental variables. Our results highlight the need to consider individual differences and to investigate multiple traits along multiple environmental axes when studying behavioral plasticity.

Sequential organization of birdsong: relationships with individual quality and fitness.

Many vocalizing animals produce the discrete elements of their acoustic signals in a specific sequential order, but we know little about the biological relevance of this ordering. For that, we must characterize the degree by which individuals differ in how they organize their signals sequentially and relate these differences to variation in quality and fitness. In this study, we fulfilled these tasks in male collared flycatchers (Ficedula albicollis). We characterized the sequential order of syllables with a network analysis approach and studied the consistency of network variables on distinct time scales (within day, between days, and between years), and assessed their relationship with such quality indicators like age, body condition, arrival date, and fitness related proxies like survival to the next year and pairing success. We found that the syllables were associated nonrandomly with one another and both the frequency differences of consecutive syllables and the number of motif types were higher in the original than in randomized syllable sequences. Average degree and small-worldness showed considerable among-individual differences and decreasing repeatability with increasing time scale. Furthermore, we found relationships between male age and average degree among and within individuals. Accordingly, older males produce syllable sequences by using common syllables less often than younger individuals. However, the network variables showed no relationship with fitness-related variables. In conclusion, the sequential organization of birdsong has the potential to encode individual-specific characteristics, which thus could be used as signal in social interactions and thus potentially could be subject to sexual selection.

Male territorial aggression and fitness in collared flycatchers: a long-term study.

Aggressive behaviour plays a fundamental role in the distribution of limiting resources. Thereby, it is expected to have consequences for fitness. Here, we explored the relationship between aggression and fitness in a long-term database collected in a wild population of the collared flycatcher (Ficedula albicollis). We quantified the aggression of males during nest-site defence by conducting simulated territorial intrusions in the courtship period. We estimated the fitness of males based on their pairing success, breeding output and survival to next year. Earlier arriving and older males had a higher probability to establish pair-bond, and males that started to breed earlier fledged more young. Aggression did not predict pairing and breeding performances. However, the probability of a male to return in the next year was significantly related to aggression in an age-dependent manner. Among subadult males, more aggressive individuals had higher chances to return, while among adult males, less aggressive ones did so. This finding is in harmony with our general observation that subadult collared flycatcher males behave more aggressively than adult males when confronted with a conspecific intruder. Subadult males may be socially inexperienced, so they should be more aggressive to be successful. In contrast, if adult males suffer from higher physiological costs, a lower level of aggression may be more advantageous for them. Our study shows that aggressive behaviour can be a fitness-related trait, and to understand its role in determining fitness, age should be taken into account.

Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population.

When mean behaviors correlate among individuals, they form behavioral syndromes. One way to understand the evolution of such a group-level phenomenon is to compare horizontally patterns of correlations among populations (or species) or follow longitudinally the same population over years in the light of parallel differences in the environment. We applied the longitudinal approach to 8-year field data and analyzed phenotypic correlations, and their within- and between-individual components, among three behaviors (novelty avoidance, aggression, and risk-taking) in male collared flycatchers, Ficedula albicollis, in a meta-analytic framework. The phenotypic correlation between novelty avoidance and aggression varied heterogeneously (it was positive in some years, while it was negative in other years), while the other pair-wise correlations were consistently positive over the study period. We investigated four potential socio-ecological factors, and found evidence that the among-year alterations in the demographic structure of the population (density, age composition) can be responsible for the heterogeneous effect sizes. Comparing within- and between-individual correlations across pairs of traits, we found that the correlation between aggression and risk-taking at the among-individual level was the strongest suggesting that this relationship has the highest potential to form a behavioral syndrome. Within-year repeatabilities varied among traits, but were systematically higher than between-year repeatabilities. Our study highlights on an empirical basis that there can be several biological and statistical reasons behind detecting a phenotypic correlation in a study, but only few of these imply that fixed behavioral syndromes are maintained in a natural population. In fact, some correlations seem to be shaped by environmental fluctuations.

Aggressive behavior of the male parent predicts brood sex ratio in a songbird.

Brood sex ratio is often affected by parental or environmental quality, presumably in an adaptive manner that is the sex that confers higher fitness benefits to the mother is overproduced. So far, studies on the role of parental quality have focused on parental morphology and attractiveness. However, another aspect, the partner's behavioral characteristics, may also be expected to play a role in brood sex ratio adjustment. To test this hypothesis, we investigated whether the proportion of sons in the brood is predicted by the level of territorial aggression displayed by the father, in the collared flycatcher (Ficedula albicollis). The proportion of sons in the brood was higher in early broods and increased with paternal tarsus length. When controlling for breeding date and body size, we found a higher proportion of sons in the brood of less aggressive fathers. Male nestlings are more sensitive to the rearing environment, and the behavior of courting males may often be used by females to assess their future parental activity. Therefore, adjusting brood sex ratio to the level of male aggression could be adaptive. Our results indicate that the behavior of the partner could indeed be a significant determinant in brood sex ratio adjustment, which should not be overlooked in future studies.

The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher.

There is increasing evidence that the genetic architecture of exploration behavior includes the dopamine receptor D4 gene (DRD4). Such a link implies that the within-individual consistency in the same behavior has a genetic basis. Behavioral consistency is also prevalent in the form of between-individual correlation of functionally different behaviors; thus, the relationship between DRD4 polymorphism and exploration may also be manifested for other behaviors. Here, in a Hungarian population of the collared flycatcher, Ficedula albicollis, we investigate how males with distinct DRD4 genotypes differ in the consistent elements of their behavioral displays during the courtship period. In completely natural conditions, we assayed novelty avoidance, aggression and risk-taking, traits that were previously shown repeatable over time and correlate with each other, suggesting that they could have a common mechanistic basis. We identified two single-nucleotide polymorphisms (SNP554 and SNP764) in the exon 3 of the DRD4 gene by sequencing a subsample, then we screened 202 individuals of both sexes for these SNPs. Focusing on the genotypic variation in courting males, we found that "AC" heterozygote individuals at the SNP764 take lower risk than the most common "AA" homozygotes (the "CC" homozygotes were not represented in our subsample of males). We also found a considerable effect size for the relationship between SNP554 polymorphism and novelty avoidance. Therefore, in addition to exploration, DRD4 polymorphisms may also be associated with the regulation of behaviors that may incur fear or stress. Moreover, polymorphisms at the two SNPs were not independent indicating a potential role for genetic constraints or another functional link, which may partially explain behavioral correlations.