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.

The estimation of additive genetic variance of body size in a wild passerine is sensitive to the method used to estimate relatedness among the individuals.

Assessing additive genetic variance is a crucial step in predicting the evolutionary response of a target trait. However, the estimated genetic variance may be sensitive to the methodology used, e.g., the way relatedness is assessed among the individuals, especially in wild populations where social pedigrees can be inaccurate. To investigate this possibility, we investigated the additive genetic variance in tarsus length, a major proxy of skeletal body size in birds. The model species was the collared flycatcher (Ficedula albicollis), a socially monogamous but genetically polygamous migratory passerine. We used two relatedness matrices to estimate the genetic variance: (1) based solely on social links and (2) a genetic similarity matrix based on a large array of single-nucleotide polymorphisms (SNPs). Depending on the relatedness matrix considered, we found moderate to high additive genetic variance and heritability estimates for tarsus length. In particular, the heritability estimates were higher when obtained with the genetic similarity matrix instead of the social pedigree. Our results confirm the potential for this crucial trait to respond to selection and highlight methodological concerns when calculating additive genetic variance and heritability in phenotypic traits. We conclude that using a social pedigree instead of a genetic similarity matrix to estimate relatedness among individuals in a genetically polygamous wild population may significantly deflate the estimates of additive genetic variation.

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.

Triparental care in the collared flycatcher (Ficedula albicollis): Cooperation of two females with a cuckolded male in rearing a brood.

Certain predominant forms of mating and parental care systems are assumed in several model species among birds, but the opportunistic and apparently infrequent variations of "family structures" may often remain hidden due to methodological limitations with regard to genetic or behavioral observations. One of the intensively studied model species, the collared flycatcher (Ficedula albicollis), is usually characterized by social monogamy with polyterritorial, facultative social polygyny, and frequent extrapair mating and extrapair paternity. During a brood-size manipulation experiment, we observed two females and a male delivering food at an enlarged brood. A combination of breeding phenology data (egg laying and hatching date), behavioral data (feeding rates) from video recordings at 10 days of nestling age, and microsatellite genotyping for maternity and paternity suggests a situation of an unrelated female helping a pair in chick rearing. Such observations highlight the relevance of using traditional techniques and genetic analyses together to assess the parental roles within a population, which becomes more important where individuals may dynamically switch from their main and presupposed roles according to the actual environmental conditions.

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.

Digit ratio predicts the number of lifetime recruits in female collared flycatchers.

The early environment in which an organism grows can have long-lasting impacts on both its phenotype and fitness. However, assessing this environment comprehensively is a formidable task. The relative length of the second to the fourth digit (2D : 4D) is a broadly studied skeletal trait that is fixed for life during ontogeny. 2D : 4D has been shown to indicate various early effects including the perinatal steroid milieu in both humans and non-human animals. However, the fitness relevance of the early effects indicated by 2D : 4D remains unknown. Here, we investigated hindlimb 2D : 4D and measures of lifetime performance in wild collared flycatcher ( Ficedula albicollis) females. We found that females with higher 2D : 4D had a greater number of recruiting offspring to the breeding population. This was the case despite the fact that such females did not lay more eggs or breed more frequently during their reproductive life. Our results support the suggestion that 2D : 4D, known to be a retrospective marker of perinatal development, positively associates with female quality in the collared flycatcher.

Reflectance variation in the blue tit crown in relation to feather structure.

Structural plumage colour is one of the most enigmatic sexually selected traits. The information content of structural colour variation is debated, and the heterogeneity of the findings is hard to explain because the proximate background of within-species colour differences is very scarcely studied. We combined measurements of feather macrostructure and nanostructure to explain within-population variability in blue tit crown reflectance. We found that sexual dichromatism in aspects of crown reflectance was explained only by feather macrostructure, whereas nanostructural predictors accounted for some of the age-related differences in reflectance. Moreover, we found that both mean reflectance and spectral shape traits reflected a combination of quantity and regularity aspects in macrostructure and nanostructure. This rich proximate background provides ample scope for reflectance to convey various types of information on individual quality.

Haemoproteus infection status of collared flycatcher males changes within a breeding season.

In ecological studies of haemosporidian parasites, prevalence is typically considered as a stable attribute. However, little is known about the possible within-host dynamics of these parasites that may originate from environmental fluctuations, parasite life cycles and the ability of hosts to suppress or clear infection. We sampled the blood of male collared flycatchers Ficedula albicollis twice within a breeding season and investigated the determinants of initial infection status and change in infection status. We found that older males tended to be initially more infected at courtship. Change in infection status was unrelated to male traits, but a widespread disappearance of Haemoproteus pallidus infection from the blood was detected between courtship and nestling rearing. The probability of change in infection status increased with the time elapsed between sampling occasions. This suggests that the disappearance of infection from the blood was due to either an active parasite suppression mechanism or the beginning of the latent phase in the parasite life cycle. Initial infection status or disappearance of infection from the blood showed no correlation with breeding success. These results show that H. pallidus infection status and thus prevalence are dynamically changing attributes and this has widespread practical and ecological implications.

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.

Laying date and polygyny as determinants of annual reproductive success in male collared flycatchers (Ficedula albicollis): a long-term study.

Annual reproductive success (ARS) is one of the main components of lifetime reproductive success, a reliable measure of individual fitness. Previous studies often dealt with ARS and variables potentially affecting it. Among them, long-term studies that consider multiple factors at the same time are particularly important in understanding the adaptive value of different phenotypes. Here, we used an 18-year dataset to quantify the ARS of male collared flycatchers (Ficedula albicollis) on the basis of recruited offspring. We simultaneously assessed the effect of start of breeding, age, polygyny, body size and the expression of forehead patch (a sexually selected trait). The success of early breeding individuals was appreciably higher than late birds; however, breeding too early was also disadvantaged, and males that bred around the yearly median breeding date had the highest ARS. Polygynous males were more successful in years with good food supply, while in years with low food availability, they did not produce more recruits than monogamous males. The age of males, their forehead patch size and body size did not affect the number of recruits. Our findings support the importance of breeding date and suggest stabilizing selection on it in the long term. We also show that polygyny is not always advantageous for males, and its fitness pay-off may depend on environmental quality.

Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher.

The possible integration of different sexual ornaments into a composite system, and especially the information content of such ornament complexes, is poorly investigated. Many bird species display complex plumage coloration, but whether this represents one integrated or several independent sexual traits can be unclear. Collared flycatchers (Ficedula albicollis) display melanised and depigmented plumage areas, and the spectral features (brightness and UV chroma) of these are correlated with each other across the plumage. In a 5-year dataset of male and female plumage reflectance, we examined some of the potential information content of integrated, plumage-level colour attributes by estimating their relationships to previous and current year body condition, laying date and clutch size. Females were in better condition the year before they became darker pigmented, and males in better current year condition were also darker pigmented. Female pigment-based brightness was positively, while male structurally based brightness was negatively related to current laying date. Finally, the overall UV chroma of white plumage areas in males was positively associated with current clutch size. Our results show that higher degree of pigmentation is related to better condition, while the structural colour component is associated with some aspects of reproductive investment. These results highlight the possibility that correlated aspects of a multiple plumage ornamentation system may reflect together some aspects of individual quality, thereby functioning as a composite signal.

Lifetime offspring production in relation to breeding lifespan, attractiveness, and mating status in male collared flycatchers.

As a comprehensive fitness parameter, lifetime reproductive success (LRS) is influenced by many different environmental and genetic factors, among which longevity is one of the most important. These factors can be reflected in secondary sexual characters, which may affect the life histories of individuals via social relations with conspecifics. Facultative polygyny in birds is another conspicuous reproductive trait that potentially increases male reproductive success, but lifetime success data in relation to polygyny are scarce. Here, we used 17 years of breeding data to quantify the LRS of male collared flycatchers (Ficedula albicollis) on the basis of lifetime recruitment of offspring. Breeding lifespan showed a positive relationship with LRS, and it was also significantly associated with mean recruitment of offspring per breeding year. Body size and sexually selected forehead patch size did not predict the number of recruits. Polygyny was positively associated with LRS, but when we corrected for lifespan, this relationship disappeared. Our results demonstrate that the relationship between longevity and LRS is not explained by the higher number of reproductive attempts when living longer, and question the adaptive value of polygyny in this population. The lack of association between forehead patch size and recruitment suggests that forehead patch is a poor indicator of phenotypic quality in our birds.

Integration of spectral reflectance across the plumage: implications for mating patterns.

BACKGROUND: In complex sexual signaling systems such as plumage color, developmental or genetic links may occur among seemingly distinct traits. However, the interrelations of such traits and the functional significance of their integration rarely have been examined. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the parallel variation of two reflectance descriptors (brightness and UV chroma) across depigmented and melanized plumage areas of collared flycatchers (Ficedula albicollis), and the possible role of integrated color signals in mate acquisition. We found moderate integration in brightness and UV chroma across the plumage, with similar correlation structures in the two sexes despite the strong sexual dichromatism. Patterns of parallel color change across the plumage were largely unrelated to ornamental white patch sizes, but they all showed strong assortative mating between the sexes. Comparing different types of assortative mating patterns for individual spectral variables suggested a distinct role for plumage-level color axes in mate acquisition. CONCLUSIONS/SIGNIFICANCE: Our results indicate that the plumage-level, parallel variation of coloration might play a role in mate acquisition. This study underlines the importance of considering potential developmental and functional integration among apparently different ornaments in studies of sexual selection.

Breeding experience and the heritability of female mate choice in collared flycatchers.

BACKGROUND: Heritability in mate preferences is assumed by models of sexual selection, and preference evolution may contribute to adaptation to changing environments. However, mate preference is difficult to measure in natural populations as detailed data on mate availability and mate sampling are usually missing. Often the only available information is the ornamentation of the actual mate. The single long-term quantitative genetic study of a wild population found low heritability in female mate ornamentation in Swedish collared flycatchers. One potentially important cause of low heritability in mate ornamentation at the population level is reduced mate preference expression among inexperienced individuals. METHODOLOGY/PRINCIPAL FINDINGS: Applying animal model analyses to 21 years of data from a Hungarian collared flycatcher population, we found that additive genetic variance was 50 percent and significant for ornament expression in males, but less than 5 percent and non-significant for mate ornamentation treated as a female trait. Female breeding experience predicted breeding date and clutch size, but mate ornamentation and its variance components were unrelated to experience. Although we detected significant area and year effects on mate ornamentation, more than 85 percent of variance in this trait remained unexplained. Moreover, the effects of area and year on mate ornamentation were also highly positively correlated between inexperienced and experienced females, thereby acting to remove difference between the two groups. CONCLUSIONS/SIGNIFICANCE: The low heritability of mate ornamentation was apparently not explained by the presence of inexperienced individuals. Our results further indicate that the expression of mate ornamentation is dominated by temporal and spatial constraints and unmeasured background factors. Future studies should reduce unexplained variance or use alternative measures of mate preference. The heritability of mate preference in the wild remains a principal but unresolved question in evolutionary ecology.

Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in Great tit nestlings, Parus major.

In nestlings, glucocorticoid (GC) secretion has short-term and long-term fitness consequences. For example, short-time elevations trigger begging activity, whereas chronically elevated GC levels impair body condition, growth and cognitive abilities. Despite a growing body of literature on personality traits, the effects of selection for fast and slow exploration on GC secretion have received little attention. We compared baseline and stress-induced hypothalamic-pituitary-adrenal (HPA) axis activity of hand-reared great tit nestlings of lines selected for fast and slow exploration. Nestling droppings were collected under three conditions: control, test (following handling stress, day 14 after hatching) and the following day. The concentrations of excreted immunoreactive corticosterone metabolites (CM) were determined via an enzyme immunoassay. We also observed nestlings' begging behaviour. CM differed significantly between the lines. Nestlings of the fast line excreted lower CM than slow-line birds. In response to handling stress, nestlings excreted significantly higher concentrations of CM than during the control and on the day after handling. Sex and begging activity were not related to CM levels. Under the control condition, but not after handling, males begged significantly more often than females. In both lines, adults excreted significantly less CM compared to nestlings. Both nestlings and adults of the slow line produced higher baseline CM values than fast-line birds. Fast-line nestlings excreted lower baseline CM than nestlings of a wild population not selected for fast or slow exploration. Slow-line nestlings did not. Our results show that selection on the basis of exploratory behaviour affected HPA axis reactivity.

Passerine extrapair mating dynamics: a bayesian modeling approach comparing four species.

In many socially monogamous animals, females engage in extrapair copulation (EPC), causing some broods to contain both within-pair and extrapair young (EPY). The proportion of all young that are EPY varies across populations and species. Because an EPC that does not result in EPY leaves no forensic trace, this variation in the proportion of EPY reflects both variation in the tendency to engage in EPC and variation in the extrapair fertilization (EPF) process across populations and species. We analyzed data on the distribution of EPY in broods of four passerines (blue tit, great tit, collared flycatcher, and pied flycatcher), with 18,564 genotyped nestlings from 2,346 broods in two to nine populations per species. Our Bayesian modeling approach estimated the underlying probability function of EPC (assumed to be a Poisson function) and conditional binomial EPF probability. We used an information theoretical approach to show that the expected distribution of EPC per female varies across populations but that EPF probabilities vary on the above-species level (tits vs. flycatchers). Hence, for these four passerines, our model suggests that the probability of an EPC mainly is determined by ecological (population-specific) conditions, whereas EPF probabilities reflect processes that are fixed above the species level.