Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird.

Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

Eco-Evolutionary Consequences of Dispersal Syndromes during Colonization in a Passerine Bird.

AbstractIn most animal species, dispersing individuals possess phenotypic attributes that mitigate the costs of colonization and/or increase settlement success in new areas (dispersal syndromes). This phenotypic integration likely affects population dynamics and the direction of selection, but data are lacking for natural populations. Using an approach that combines population dynamics, quantitative genetics, and phenotypic selection analyses, we reveal the existence of dispersal syndromes in a pied flycatcher (Ficedula hypoleuca) population in the Netherlands: immigrants were larger, tended to have darker plumage, bred earlier, and produced larger clutches than local recruits, and some of these traits were genetically correlated. Over time, the phenotypic profile of the population gradually changed: each generation advanced arrival and breeding and exhibited longer wings as a result of direct and indirect selection on these correlated traits. Although phenotypic attributes of immigrants were favored by selection during the early phase of colonization, observed phenotypic changes were similar for immigrants and local recruits. We propose that immigrants facilitated initial population establishment but that temporal changes likely resulted from climate change-induced large-scale selection. This study highlights that newly established populations are of nonrandom composition and that phenotypic architecture affects evolutionary population trajectories.

Unravelling the causes and consequences of dispersal syndromes in a wild passerine.

Evidence accumulates that dispersal is correlated with individual behavioural phenotype (dispersal syndrome). The evolutionary causes and consequences of such covariation depend on the degree of plasticity versus inheritance of the traits, which requires challenging experiments to implement in mobile organisms. Here, we combine a forced dispersal experiment, natural colonization and longitudinal data to establish if dispersal and aggression levels are integrated and to test their adaptive nature in pied flycatchers (Ficedula hypoleuca). We found that (forced) dispersers behaved more aggressively in their first breeding year after dispersal and decreased their aggression in following years. Strength of dispersal syndrome and direction of fecundity selection on aggression in newly colonized areas varied between years. We propose that the net benefits of aggression for dispersers increase under harsh conditions (e.g. low food abundance). This hypothesis now warrants further testing. Overall, this study provides unprecedented experimental evidence that dispersal syndromes can be remodelled via adaptive plasticity depending on the individuals' local breeding experience and/or year-specific ecological conditions. It highlights the importance of individual behavioural variation in population dynamics.

State dependence explains individual variation in nest defence behaviour in a long-lived bird.

Parental care, such as nest or offspring defence, is crucial for offspring survival in many species. Yet, despite its obvious fitness benefits, the level of defence can consistently vary between individuals of the same species. One prominent adaptive explanation for consistent individual differences in behaviours involves state dependency: relatively stable differences in individual state should lead to the emergence of repeatable behavioural variation whereas changes in state should lead to a readjustment of behaviour. Therefore, empirical testing of adaptive state dependence requires longitudinal data where behaviour and state of individuals of the same population are repeatedly measured. Here, we test if variation in states predicts nest defence behaviour (a 'risky' behaviour) in a long-lived species, the barnacle goose Branta leucopsis. Adaptive models have predicted that an individual's residual reproductive value or 'asset' is an important state variable underlying variation in risk-taking behaviour. Hence, we investigate how nest defence varies as a function of time of the season and individual age, two state variables that can vary between and within individuals and determine asset. Repeated measures of nest defence towards a human intruder (flight initiation distance or FID) of females of known age were collected during 15 breeding seasons. Increasing values of FID represent increasing shyness. We found that females strongly and consistently differed in FID within- and between-years. As predicted by theory, females adjusted their behaviour to state by decreasing their FID with season and age. Decomposing these population patterns into within- and between-individual effects showed that the state-dependent change in FID was driven by individual plasticity in FID and that bolder females were more plastic than shyer females. This study shows that nest defence behaviour differs consistently among individuals and is adjusted to individual state in a direction predicted by adaptive personality theory.

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird.

Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality-related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density-dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.

Does coping style predict optimization? An experimental test in a wild passerine bird.

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, 'proactive' individuals who do not track environmental changes may be less able to produce optimal brood sizes than 'reactive' individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.

Effects of early predation and social cues on the relationship between laterality and personality.

Individual differences in laterality and personality are expected to covary, as emotions are processed differently by the two hemispheres, and personality involves emotional behavior. Fish species are often used to investigate this topic due to the large variability in personality and laterality patterns. While some species show a positive relationship between lateralization strength and boldness, others show a negative relationship, and some show no relationship. A new way to assess the robustness of such a relationship is to manipulate both laterality and personality to examine how this affects their relationship. To this end, we conducted a fully factorial design experiment manipulating predation and group size during early development. Results showed that the strength of laterality was influenced by predation threat, while social tendency and boldness were influenced by group size. These findings suggest that early life conditions can have an impact on laterality and social behavior. The relationship between laterality and personality traits, while present, was heavily influenced by the specific trial conditions but not by the different developmental conditions. In summary, the relationship between laterality and behaviors appears to be context-dependent, yet resilient to early environmental manipulations.

Adaptation to climate change through dispersal and inherited timing in an avian migrant.

Many organisms fail to adjust their phenology sufficiently to climate change. Studies have concentrated on adaptive responses within localities, but little is known about how latitudinal dispersal enhances evolutionary potential. Rapid adaptation is expected if dispersers from lower latitudes have improved synchrony to northern conditions, thereby gain fitness and introduce genotypes on which selection acts. Here we provide experimental evidence that dispersal in an avian migrant enables rapid evolutionary adaptation. We translocated Dutch female pied flycatchers (Ficedula hypoleuca) and eggs to Sweden, where breeding phenology is ~15 days later. Translocated females bred earlier, and their fitness was 2.5 times higher than local Swedish flycatchers. We show that between-population variation in timing traits is highly heritable, and hence immigration of southern genotypes promotes the necessary evolutionary response. We conclude that studies on adaptation to large-scale environmental change should not just focus on plasticity and evolution based on standing genetic variation but should also include phenotype-habitat matching through dispersal as a viable route to adjust.

Experimental evidence for adaptive personalities in a wild passerine bird.

Individuals of the same species differ consistently in risky actions. Such 'animal personality' variation is intriguing because behavioural flexibility is often assumed to be the norm. Recent theory predicts that between-individual differences in propensity to take risks should evolve if individuals differ in future fitness expectations: individuals with high long-term fitness expectations (i.e. that have much to lose) should behave consistently more cautious than individuals with lower expectations. Consequently, any manipulation of future fitness expectations should result in within-individual changes in risky behaviour in the direction predicted by this adaptive theory. We tested this prediction and confirmed experimentally that individuals indeed adjust their 'exploration behaviour', a proxy for risk-taking behaviour, to their future fitness expectations. We show for wild great tits (Parus major) that individuals with experimentally decreased survival probability become faster explorers (i.e. increase risk-taking behaviour) compared to individuals with increased survival probability. We also show, using quantitative genetics approaches, that non-genetic effects (i.e. permanent environment effects) underpin adaptive personality variation in this species. This study thereby confirms a key prediction of adaptive personality theory based on life-history trade-offs, and implies that selection may indeed favour the evolution of personalities in situations where individuals differ in future fitness expectations.

Social environment affects juvenile dispersal in great tits (Parus major).

1. Habitat selection can affect individual fitness, and therefore, individuals are expected to assess habitat quality of potential breeding sites before settlement. 2. We investigated the role of social environment on juvenile dispersal behaviour in the great tit (Parus major). Two main contradictory hypotheses can be formulated regarding social effects on juvenile dispersal as follows: (i) High fledgling density and sex ratio may enhance the intensity of local (kin) competition and, therefore, reduce individual survival chance, enhance emigration and reduce settlement ('repulsion' hypothesis) (ii) Alternatively, high fledgling density and sex ratio may signal high-quality habitat or lead to aggregation and thus increase individual survival chance, reduce emigration and enhance settlement ('attraction' hypothesis). 3. To disentangle positive from negative effects of high density and male-biased sex ratio on dispersal, we manipulated the social composition of the fledgling population in 12 semi-isolated nest-box areas (plots) via a change of fledgling density (low/high) as well as fledgling sex ratio (female-biased/balanced/male-biased) across 3 years. We then tested whether experimental variation in male and female fledgling densities affected variation in local survival, emigration and settlement of juveniles, and whether social effects on survival and dispersal support the 'repulsion' or 'attraction' hypothesis. 4. We found no experimental effects on local survival and emigration probabilities. However, consistent with the 'attraction' hypothesis, settlement was significantly and positively affected by local experimental sex ratio in each of the study years: both male and female juveniles avoided female-biased plots and settled more in plots that were balanced and male-biased the previous year. 5. Our study provides unprecedented experimental evidence that local sex ratio plays a causal role in habitat selection. We suggest that settlers avoid female-biased plots because a high proportion of females may reflect the absence or the low quality of local resources in the habitat. Alternatively, male territory acquisition may be facilitated by a high local density of 'candidate' males, and therefore, juveniles were less successful in settling in female-biased plots.

Local sex ratio affects the cost of reproduction.

1. Costs and benefits of reproduction are central to life-history theory, and the outcome of reproductive trade-offs may depend greatly on the ecological conditions in which they are estimated. In this study, we propose that costs and benefits of reproduction are modulated by social effects, and consequently that selection on reproductive rates depends on the social environment. 2. We tested this hypothesis in a great tit Parus major population. Over 3 years, we altered parental reproductive effort via brood size manipulations (small, intermediate, large) and manipulated the local social environment via changes in the local fledgling density (decreased, increased) and the local sex ratio (female-biased, control, male-biased). 3. We found that male-biased treatment consistently increased the subsequent local breeding densities over the 3-year study period. We also found that parents rearing small broods in these male-biased plots had increased survival rates compared with the other experimental groups. 4. We conclude that reproductive costs are the product of an interaction between parental phenotypic quality after reproduction and the social environment: raising a small brood had long-lasting effects on some phenotypic traits of the parents and that this increased their survival chances in male-biased environment where habitat quality may have deteriorated (via increased disease/predation risk or intraspecific competition). 5. Our results provide the first experimental evidence that local sex ratio can affect reproductive costs and thus optimal clutch size.

DNA metabarcoding quantifies the relative biomass of arthropod taxa in songbird diets: Validation with camera-recorded diets.

Ecological research is often hampered by the inability to quantify animal diets. Diet composition can be tracked through DNA metabarcoding of fecal samples, but whether (complex) diets can be quantitatively determined with metabarcoding is still debated and needs validation using free-living animals. This study validates that DNA metabarcoding of feces can retrieve actual ingested taxa, and most importantly, that read numbers retrieved from sequencing can also be used to quantify the relative biomass of dietary taxa. Validation was done with the hole-nesting insectivorous Pied Flycatcher whose diet was quantified using camera footage. Size-adjusted counts of food items delivered to nestlings were used as a proxy for provided biomass of prey orders and families, and subsequently, nestling feces were assessed through DNA metabarcoding. To explore potential effects of digestion, gizzard and lower intestine samples of freshly collected birds were subjected to DNA metabarcoding. For metabarcoding with Cytochrome Oxidase subunit I (COI), we modified published invertebrate COI primers LCO1490 and HCO1777, which reduced host reads to 0.03%, and amplified Arachnida DNA without significant changing the recovery of other arthropod taxa. DNA metabarcoding retrieved all commonly camera-recorded taxa. Overall, and in each replicate year (N = 3), the relative scaled biomass of prey taxa and COI read numbers correlated at R = .85 (95CI:0.68-0.94) at order level and at R = .75 (CI:0.67-0.82) at family level. Similarity in arthropod community composition between gizzard and intestines suggested limited digestive bias. This DNA metabarcoding validation demonstrates that quantitative analyses of arthropod diet is possible. We discuss the ecological applications for insectivorous birds.

No experimental evidence for local competition in the nestling phase as a driving force for density-dependent avian clutch size.

1. In birds, local competition for food between pairs during the nestling phase may affect nestling growth and survival. A decrease in clutch size with an increase in breeding density could be an adaptive response to this competition. To investigate whether breeding density causally affected the clutch size of great tits (Parus major), we manipulated breeding density in three out of eight study plots by increasing nest-box densities. We expected clutch size in these plots to be reduced compared to that in control plots. 2. We analysed both the effects of variation in annual mean density (between-year comparisons) and experimental density (within-year comparison between plots) on clutch size variation, the occurrence of second broods and nestling growth. We examined within-female variation in clutch size to determine whether individual responses explain the variation over years. 3. Over the 11 years, population breeding density increased (from 0.33 to 0.50 pairs ha(-1)) while clutch size and the occurrence of second broods decreased (respectively from 10.0 to 8.5 eggs and from 0.39 to 0.05), consistent with a negative density-dependent effect for the whole population. Nestling growth showed a declining but nonsignificant trend over years. 4. The decline in population clutch size over years was primarily explained by changes occurring within individuals rather than selective disappearance of individuals laying large clutches. 5. Within years, breeding density differed significantly between manipulated plots (0.16 pairs ha(-1) vs. 0.77 pairs ha(-1)) but clutch size, occurrence of second broods and nestling growth were not affected by the experimental treatment, resulting in a discrepancy between the effects of experimental and annual variation in density on reproduction. 6. We discuss two hypotheses that could explain this discrepancy: (i) the decline in breeding performance over time was not due to density, but resulted from other, unknown factors. (ii) Density did cause the decline in breeding performance, but this was not due to local competition in the nestling phase. Instead, we suggest that competition acting in a different phase (e.g. before egg laying or after fledgling) was responsible for the density effect on clutch size among years.

Sex-specific effects of altered competition on nestling growth and survival: an experimental manipulation of brood size and sex ratio.

1. An increase of competition among adults or nestlings usually negatively affects breeding output. Yet little is known about the differential effects that competition has on the offspring sexes. This could be important because it may influence parental reproductive decisions. 2. In sexual size dimorphic species, two main contradictory mechanisms are proposed regarding sex-specific effects of competition on nestling performance assuming that parents do not feed their chicks differentially: (i) the larger sex requires more resources to grow and is more sensitive to a deterioration of the rearing conditions ('costly sex hypothesis'); (ii) the larger sex has a competitive advantage in intra-brood competition and performs better under adverse conditions ('competitive advantage hypothesis'). 3. In the present study, we manipulated the level of sex-specific sibling competition in a great tit population (Parus major) by altering simultaneously the brood size and the brood sex ratio on two levels: the nest (competition for food among nestlings) and the woodlot where the parents breed (competition for food among adults). We investigated whether altered competition during the nestling phase affected nestling growth traits and survival in the nest and whether the effects differed between males, the larger sex, and females. 4. We found a strong negative and sex-specific effect of experimental brood size on all the nestling traits. In enlarged broods, sexual size dimorphism was smaller which may have resulted from biased mortality towards the less competitive individuals i.e. females of low condition. No effect of brood sex ratio on nestling growth traits was found. 5. Negative brood size effects on nestling traits were stronger in natural high-density areas but we could not confirm this experimentally. 6. Our results did not support the 'costly sex hypothesis' because males did not suffer from higher mortality under harsh conditions. The 'competitive advantage hypothesis' was also not fully supported because females did not suffer more in male-biased broods. 7. We conclude that male nestlings are not likely to be more expensive to raise, yet they have a size-related competitive advantage in large broods, leading to higher mortality of their on average lighter female nest mates.

Effects of manipulated levels of predation threat on parental provisioning and nestling begging.

Parental provisioning behavior is a major determinant of offspring growth and survival, but high provisioning rates might come at the cost of increased predation threat. Parents should thus adjust provisioning activity according to current predation threat levels. Moreover, life-history theory predicts that response to predation threat should be correlated with investment in current reproduction. We experimentally manipulated perceived predation threat in free-living great tits (Parus major) by presenting parents with a nest predator model while monitoring different aspects of provisioning behavior and nestling begging. Experiments were conducted in 2 years differing greatly in ecological conditions, including food availability. We further quantified male territorial aggressiveness and male and female exploratory tendency. Parents adjusted provisioning according to current levels of threat in an apparently adaptive way. They delayed nest visits during periods of elevated perceived predation threat and subsequently compensated for lost feeding opportunities by increasing provisioning once the immediate threat had diminished. Nestling begging increased after elevated levels of predation threat, but returned to baseline levels by the end of the experiment, suggesting that parents had fully compensated for lost feeding opportunities. There was no evidence for a link between male exploration behavior or aggressiveness and provisioning behavior. In contrast, fast-exploring females provisioned at higher rates, but only in the year with poor environmental conditions, which might indicate a greater willingness to invest in current reproduction in general. Future work should assess whether these personality-related differences in delivery rates under harsher conditions came at a cost of reduced residual reproductive value.

Comparing the consequences of natural selection, adaptive phenotypic plasticity, and matching habitat choice for phenotype-environment matching, population genetic structure, and reproductive isolation in meta-populations.

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual-based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.

Sources of (co)variation in alternative siring routes available to male great tits (Parus major).

Males of socially monogamous species can increase their siring success via within-pair and extra-pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five-year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as "interactive phenotypes" arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra-pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra-pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.

Sex-specific effects of the local social environment on juvenile post-fledging dispersal in great tits.

An individual's decision to disperse from the natal habitat can affect its future fitness prospects. Especially in species with sex-biased dispersal, we expect the cost-benefit balance for dispersal to vary according to the social environment (e.g., local sex ratio and density). However, little is known about the social factors affecting dispersal decisions and about the temporal and spatial patterns of the dispersal process. In our study, we investigated experimentally the effects of the social environment on post-fledging dispersal of juvenile great tits by simultaneously manipulating the density and sex ratio of fledglings within forest plots. We expected young females in the post-fledging period mainly to compete for resources related to food and, as they are subordinate to males, we predicted higher female dispersal from male-biased plots. Juvenile males compete for vacant territories already in late summer and autumn; thus, we predicted increased male dispersal from high density and male-biased plots. We found that juvenile females had a higher probability to leave male-biased plots and had dispersed further from male-biased plots in the later post-fledging phase when juvenile males start to become territorial and more aggressive. Juvenile males were least likely to leave male-biased plots and had smallest dispersal distances from female-biased plots early after fledging. The results suggest that the social environment differentially affected the costs and benefits of philopatry for male and female juveniles. The local sex ratio of individuals is thus an important social trait to be considered for understanding sex-specific dispersal processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-011-1207-1) contains supplementary material, which is available to authorized users.