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.

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.

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.

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.

MHC-mediated sexual selection on birdsong: Generic polymorphism, particular alleles and acoustic signals.

Several hypotheses predict that the major histocompatibility complex (MHC) drives mating preference in females. Olfactory, colour or morphological traits are often found as reliable signals of the MHC profile, but the role of avian song mediating MHC-based female choice remains largely unexplored. We investigated the relationship between several MHC and acoustic features in the collared flycatcher (Ficedula albicollis), a European passerine with complex songs. We screened a fragment of the class IIB second exon of the MHC molecule, of which individuals harbour 4-15 alleles, while considerable sequence diversity is maintained at the population level. To make statistical inferences from a large number of comparisons, we adopted both null-hypothesis testing and effect size framework in combination with randomization procedures. After controlling for potential confounding factors, neither MHC allelic diversity nor the presence of particular alleles was associated remarkably with the investigated qualitative and quantitative song traits. Furthermore, genetic similarity among males based on MHC sequences was not reflected by the similarity in their song based on syllable content. Overall, these results suggest that the relationship between features of song and the allelic composition and diversity of MHC is not strong in the studied species. However, a biologically motivated analysis revealed that individuals that harbour an MHC allele that impairs survival perform songs with broader frequency range. This finding suggests that certain aspects of the song may bear reliable information concerning the MHC profile of the individuals, which can be used by females to optimize mate choice.

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.

Direct benefits of mate choice: a meta-analysis of plumage colour and offspring feeding rates in birds.

Mate choice is generally costly to the choosy sex, so fitness benefits must counterbalance these costs. Genetic benefits of choice are widely examined and have received overall support. Direct benefits such as high quality parental care by highly ornamented individuals are widely assumed to be important but are less frequently tested, theoretically debated, and their support in the recent literature is unknown. Furthermore, in taxa where both sexes provide care, the preferential investment of the partner in relation to ornamentation may reduce own investment and modify apparent parental care quality. In a phylogenetically controlled meta-analysis, we collated correlative results from birds concerning parental plumage coloration and the nestling feeding rates of the ornament bearer and its partner. Overall evidence was weak for signalling of parental care quality and somewhat stronger for preferential partner investment. Surprisingly, the sex of the signaller and the type of plumage colour seemed to exert weak effects on the signalling of parental care quality. Finally, there was a group of cases with opposite relationships of care and ornamentation in the two parties. We found that this group arose predominately from preferential partner investment in relation to ornamentation, with concomitant, but weaker, reduction of own investment. We conclude that the effect of partner investment on parental care indication seems system-specific and needs further study.

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.

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.

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.

Plumage color degradation indicates reproductive effort: an experiment.

Plumage color has traditionally been regarded as a static ornamental trait, but evidence is accumulating for significant color changes without molt that typically reduce the conspicuousness of ornamentation. In some species, the social partner seems to increase its reproductive investment if the color trait is experimentally enhanced, suggesting that color change could act as a signal. However, the information content of this signal is so far unclear. For example, birds in poor condition or making greater effort may deteriorate more severely. We used brood size manipulations to alter the reproductive effort of male and female collared flycatchers Ficedula albicollis. Both sexes showed less severe decline in some reflectance attribute of their white breast when their brood was experimentally reduced. In each sex, greater deterioration of the reflectance trait affected by the manipulation was accompanied by increased feeding rate by the partner. These feeding patterns do not prove, but are consistent with, a compensatory response by the partner to induced degradation. The manipulation effects on color change we detected confirm for the first time that plumage color deterioration can indicate current reproductive effort, thereby providing a potential fitness advantage to social partners that react to such deterioration.

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.

The effect of social environment on bird song: listener-specific expression of a sexual signal.

Animal signals should consistently differ among individuals to convey distinguishable information about the signalers. However, behavioral display signals, such as bird song are also loaded with considerable within-individual variance with mostly unknown function. We hypothesized that the immediate social environment may play a role in mediating such variance component, and investigated in the collared flycatcher (Ficedula albicollis) if the identity and quality of listeners could affect song production in signalers. After presenting territorial males with either a female or male social stimulus, we found in the subsequent song recordings that the among-stimulus effects corresponded to non-zero variance components in several acoustic traits indicating that singing males are able to plastically adjust their songs according to stimulus identity. Male and female stimuli elicited different responses as the identity of the female stimuli affected song complexity only, while the identity of male stimuli altered also song length, maximum frequency, and song rate. The stimulus-specific effect on song in some cases decreased with time, being particularly detectable right after the removal of the stimulus and ceasing later, but this pattern varied across the sex of the stimulus and the song traits. We were able to identify factors that can explain the among-stimulus effects (e.g., size and quality of the stimuli) with roles that also varied among song traits. Our results confirm that the variable social environment can raise considerable variation in song performance, highlighting that within-individual plasticity of bird song can play important roles in sexual signaling.

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.

Melanin-based ornament darkness positively correlates with across-season nutritional condition.

Sexually dimorphic ornamental traits are widely regarded as indicators of nutritional condition. However, variation of nutritional condition outside the reproductive and the ornament production seasons has rarely been considered, although it affects the generality of information content, especially for ornaments that may be used across the year. We measured several indicators of migratory and molt condition in male and female blackcaps (Sylvia atricapilla) during their autumn migration, and quantified their crown reflectance. We detected robust correlations between migratory and molt condition indices, and the correlation structure was similar in the two sexes. Furthermore, the across-season measure of body condition was positively related to the darkness of the black crown in males, while being unrelated to reflectance traits of the reddish crown in females. Our results reinforce the possibility that some melanin-based ornaments may be year-round indicators of individual quality via their dependence on nutritional condition.

Elemental composition in feathers of a migratory passerine for differentiation of sex, age, and molting areas.

The bulk analysis of single feathers of 263 feathers belonging to 238 individuals of a migratory passerine (collared flycatcher, Ficedula albicollis, originating from a breeding population in the Pilis-Visegrád Mountains in Hungary) by inductively coupled plasma sector field mass spectrometry (ICP-SF-MS) for determination of elements after proper dissolution allowed the quantitative determination of 38 elements. Calcium, Mg, Mn, Fe, and Zn were found to have a quantitative determination frequency larger than 80 % and a concentration greater than 100 µg/g. Among ecotoxicologically relevant elements, Ni, Cd, Hg, and Pb could be determined in more than 55 % of the tail feather samples. The concentration of Hg with a quantification limit of 0.006 µg/g and Pb with that of 0.015 µg/g was higher than 1 and 10 µg/g, respectively, in more than 80 % of the investigated samples, but generally lower than levels that could cause adverse behavioral effects. The principal component analyses of elemental concentration data followed by the application of general linear models revealed that, for male collared flycatchers, the concentration of Sn, Pb, Ni, Sr, Mg, Zn, Ba, and Sc differed significantly in the wing and tail feathers collected from the same individuals. With females, only the Ca and Sc concentration showed a significant difference between wing and tail feathers. Moreover, the concentration of rare earth elements, V, Fe, Sr, Mg, Mn, Zn, Pb, and Ba in tail feathers allowed differentiation between sexes while the concentration of Se, Bi, and Sc between yearling and adult male individuals. At the same time, Sc differentiated age categories in females. Distribution of major elements along the rachis of feathers could be monitored by laser ablation ICP-SF-MS after normalization of the intensities to either 13C or 34S signals.

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.