Wild Population Of Great Tits Research Articles

No relationship between chronotype and timing of breeding when variation in daily activity patterns across the breeding season is taken into account.

There is increasing evidence that individuals are consistent in the timing of their daily activities, and that individual variation in temporal behavior is related to the timing of reproduction. However, it remains unclear whether observed patterns relate to the timing of the onset of activity or whether an early onset of activity extends the time that is available for foraging. This may then again facilitate reproduction. Furthermore, the timing of activity onset and offset may vary across the breeding season, which may complicate studying the above‐mentioned relationships. Here, we examined in a wild population of great tits (Parus major) whether an early clutch initiation date may be related to an early onset of activity and/or to longer active daylengths. We also investigated how these parameters are affected by the date of measurement. To test these hypotheses, we measured emergence and entry time from/into the nest box as proxies for activity onset and offset in females during the egg laying phase. We then determined active daylength. Both emergence time and active daylength were related to clutch initiation date. However, a more detailed analysis showed that the timing of activities with respect to sunrise and sunset varied throughout the breeding season both within and among individuals. The observed positive relationships are hence potentially statistical artifacts. After methodologically correcting for this date effect, by using data from the pre‐egg laying phase, where all individuals were measured on the same days, neither of the relationships remained significant. Taking methodological pitfalls and temporal variation into account may hence be crucial for understanding the significance of chronotypes.

Prior experience of captivity affects behavioural responses to 'novel' environments.

Information ecology theory predicts that prior experience influences current behaviour, even if the information is acquired under a different context. However, when individuals are tested to quantify personality, cognition, or stress, we usually assume that the novelty of the test is consistent among individuals. Surprisingly, this ‘gambit of prior experience’ has rarely been explored. Therefore, here we make use of a wild population of great tits (Parus major) to test if prior experience of handling and captivity influences common measures of exploration (open field tests in two novel contexts: room and cage arenas), social response (simulated using a mirror), and behavioural stress (breathing rate). We found that birds with prior experience of captivity (caught previously for unrelated learning and foraging experiments) were more exploratory, but this depended on age: exploration and captivity experience (in terms of both absolute binary experience and the length of time spent in captivity) were associated more strongly in young (first-winter) birds than in adults. However, there was no association of prior experience of captivity with social response and breathing rate, and nor did the measures of exploration correlate. Together our results suggest that re-testing of individuals requires careful consideration, particularly for younger birds, and previous experiences can carry over and affect behaviours differently.

The effect of experimental lead pollution on DNA methylation in a wild bird population

ABSTRACT Anthropogenic pollution is known to negatively influence an organism’s physiology, behaviour, and fitness. Epigenetic regulation, such as DNA methylation, has been hypothesized as a potential mechanism to mediate such effects, yet studies in wild species are lacking. We first investigated the effects of early-life exposure to the heavy metal lead (Pb) on DNA methylation levels in a wild population of great tits (Parus major), by experimentally exposing nestlings to Pb at environmentally relevant levels. Secondly, we compared nestling DNA methylation from a population exposed to long-term heavy metal pollution (close to a copper smelter), where birds suffer from pollution-related decrease in food quality, and a control population. For both comparisons, the analysis of about one million CpGs covering most of the annotated genes revealed that pollution-related changes in DNA methylation were not genome wide, but enriched for genes underlying developmental processes. However, the results were not consistent when using binomial or beta binomial regression highlighting the difficulty of modelling variance in CpGs. Our study indicates that post-natal anthropogenic heavy metal exposure can affect methylation levels of development related genes in a wild bird population.

Strong phenotypic trait correlations between mating partners do not result from assortative mating in wild great tits (Parus major)

There is considerable debate about the occurrence of assortative mating between phenotypic traits measured within natural populations. Meta-analyses have implied that assortative mating occurs generally in natural populations, but recent work indicates these conclusions largely result from biased data. Specifically, estimates of phenotypic correlations between mating partners do not solely result from nonrandom associations between individual-level traits of partners but also from other biological processes (joint phenotypic plasticity, indirect genetic effects), methodological practices (observer bias) and other unexplained residual correlations (e.g. correlated measurement error). This paper puts this critique to test. First, we estimated the overall phenotypic correlation between phenotypic traits of mating partners for a wild population of great tits. Second, we estimated various key variance components to reveal the extent to which phenotypic correlations between partners resulted from assortative mating, reversible plasticity, social partner effects and methodological practices. We performed our analyses for a range of phenotypic traits (body mass, breathing rate, exploration behaviour, wing and tarsus length) to derive general conclusions not hinging on the specifics of the traits involved. Our analyses support the conclusion that patterns of assortative mating exist at first glance but occur because of the biasing effects of correlated residuals likely caused by a combination of phenotypic responses to unknown environmental factors or measurement error-not because of intrinsic patterns of assortative mating.

Repeatable differences in exploratory behaviour predict tick infestation probability in wild great tits

Ecological factors and individual-specific traits affect parasite infestation in wild animals. Ixodid ticks are important ectoparasites of various vertebrate hosts, which include passerine bird species such as the great tit (Parus major). We studied various key ecological variables (breeding density, human disturbance) and phenotypic traits (exploratory behaviour, body condition) proposed to predict tick infestation probability and burden in great tits. Our study spanned 3 years and 12 nest box plots located in southern Germany. Breeding, adult great tits were assessed for exploration behaviour, body condition, and tick burden. Plots were open to human recreation; human disturbance was quantified in each plot as a recreation pressure index from biweekly nest box inspections. Infested individuals were repeatable in tick burden across years. These repeatable among-individual differences in tick burden were not attributable to exploration behaviour. However, faster explorers did have a higher infestation probability. Furthermore, body condition was negatively correlated to tick burden. Recreation pressure was correlated to increased infestation probability, although this relationship was just above the threshold of statistical significance. Our study implies that avian infestation probability and tick burden are each determined by distinct phenotypic traits and ecological factors. Our findings highlight the importance of animal behaviour and human disturbance in understanding variation in tick burden among avian hosts.Significance statementVarious abiotic and biotic factors, including personality type, influence tick parasitism in birds, but exactly how all these factors interplay remains unclear. We studied a wild population of great tits over a 3-year period and assessed birds for their exploration behaviour and tick infestation. We found that more explorative great tits were more likely to be infested with ticks. By contrast, faster explorers did not have higher tick burdens. Tick burden was nevertheless moderately repeatable among individuals. Our results imply that animal personality influences the probability of parasite infestation, and that infestation likelihood versus intensity are determined by distinct mechanisms. Our work highlights the importance of animal behaviour to understand parasite infestation in wild populations.

Novel sources of (co)variation in nestling begging behavior and hunger at different biological levels of analysis

Abstract Biological hypotheses predicting patterns of offspring begging typically concern the covariance with hunger and/or development at specific hierarchical levels. For example, hunger drives within-individual patterns of begging, but begging also drives food intake among individuals within broods, and begging and food intake can covary positively or negatively among genotypes or broods. Testing biological phenomena that occur at multiple levels, therefore, requires the partitioning of covariance between traits of interest to ensure that each level-specific relationship is appropriately assessed. We performed a partial cross-fostering study on a wild population of great tits (Parus major), then used multivariate mixed models to partition variation and covariation in nestling begging effort and two metrics of nestling hunger within versus among individual nestlings and broods. At the within-individual level, we found that nestlings begged more intensely when hungrier (positive correlation between begging and hunger). However, among individuals, nestlings that were fed more frequently also begged more intensely on average (negative correlation between begging and hunger). Variation in nestling mass did not give rise to the negative correlation between begging and hunger among nestlings, but we did find that lighter nestlings begged more intensely than their heavier biological siblings, suggesting that this effect may be driven by a genetic component linked to offspring size. Our study illustrates how patterns of covariance can differ across biological levels of analysis and addresses biological mechanisms that could produce these previously obscured patterns.

Partner’s age, not social environment, predicts extrapair paternity in wild great tits (Parus major)

Abstract An individual’s fitness is not only influenced by its own phenotype, but by the phenotypes of interacting conspecifics. This is likely to be particularly true when considering fitness gains and losses caused by extrapair matings, as they depend directly on the social environment. While previous work has explored effects of dyadic interactions, limited understanding exists regarding how group-level characteristics of the social environment affect extrapair paternity (EPP) and cuckoldry. We use a wild population of great tits (Parus major) to examine how, in addition to the phenotypes of focal parents, two neighborhood-level traits—age and personality composition—predict EPP and cuckoldry. We used the well-studied trait “exploration behavior” as a measure of the reactive-proactive personality axis. Because breeding pairs inhabit a continuous “social landscape,” we first established an ecologically relevant definition of a breeding “neighborhood” through genotyping parents and nestlings in a 51-ha patch of woodland and assessing the spatial predictors of EPP events. Using the observed decline in likelihood of EPP with increasing spatial separation between nests, we determined the relevant neighborhood boundaries, and thus the group phenotypic composition of an individual’s neighborhood, by calculating the point at which the likelihood of EPP became negligible. We found no evidence that “social environment” effects (i.e., neighborhood age or personality composition) influenced EPP or cuckoldry. We did, however, find that a female’s own age influenced the EPP of her social mate, with males paired to older females gaining more EPP, even when controlling for the social environment. These findings suggest that partner characteristics, rather than group phenotypic composition, influence mating activity patterns at the individual level.

Exploratory behavior undergoes genotype-age interactions in a wild bird.

Animal personality traits are often heritable and plastic at the same time. Indeed, behaviors that reflect an individual's personality can respond to environmental factors or change with age. To date, little is known regarding personality changes during a wild animals' lifetime and even less about stability in heritability of behavior across ages. In this study, we investigated age‐related changes in the mean and in the additive genetic variance of exploratory behavior, a commonly used measure of animal personality, in a wild population of great tits. Heritability of exploration is reduced in adults compared to juveniles, with a low genetic correlation across these age classes. A random regression animal model confirmed the occurrence of genotype–age interactions (G×A) in exploration, causing a decrease in additive genetic variance before individuals become 1 year old, and a decline in cross‐age genetic correlations between young and increasingly old individuals. Of the few studies investigating G×A in behaviors, this study provides rare evidence for this phenomenon in an extensively studied behavior. We indeed demonstrate that heritability and cross‐age genetic correlations in this behavior are not stable over an individual's lifetime, which can affect its potential response to selection. Because G×A is likely to be common in behaviors and have consequences for our understanding of the evolution of animal personality, more attention should be turned to this phenomenon in the future work.

Incubation behavior adjustments, driven by ambient temperature variation, improve synchrony between hatch dates and caterpillar peak in a wild bird population.

For organisms living in seasonal environments, synchronizing the peak energetic demands of reproduction with peak food availability is a key challenge. Understanding the extent to which animals can adjust behavior to optimize reproductive timing, and the cues they use to do this, is essential for predicting how they will respond to future climate change. In birds, the timing of peak energetic demand is largely determined by the timing of clutch initiation; however, considerable alterations can still occur once egg laying has begun. Here, we use a wild population of great tits (Parus major) to quantify individual variation in different aspects of incubation behavior (onset, duration, and daily intensity) and conduct a comprehensive assessment of the causes and consequences of this variation. Using a 54‐year dataset, we demonstrate that timing of hatching relative to peak prey abundance (synchrony) is a better predictor of reproductive success than clutch initiation or clutch completion timing, suggesting adjustments to reproductive timing via incubation are adaptive in this species. Using detailed in‐nest temperature recordings, we found that postlaying, birds improved their synchrony with the food peak primarily by varying the onset of incubation, with duration changes playing a lesser role. We then used a sliding time window approach to explore which spring temperature cues best predict variance in each aspect of incubation behavior. Variation in the onset of incubation correlated with mean temperatures just prior to laying; however, incubation duration could not be explained by any of our temperature variables. Daily incubation intensity varied in response to daily maximum temperatures throughout incubation, suggesting female great tits respond to temperature cues even in late stages of incubation. Our results suggest that multiple aspects of the breeding cycle influence the final timing of peak energetic demand. Such adjustments could compensate, in part, for poor initial timing, which has significant fitness impacts.

Effect of an anti-malaria drug on behavioural performance on a problem-solving task: An experiment in wild great tits

Malaria parasites have been shown to decrease host fitness in several species in the wild and their detrimental effects on host cognitive ability are well established in humans. However, experimental demonstrations of detrimental effects on non-human host behaviour are currently limited. In this study, we experimentally tested whether injections of an anti-malaria drug affected short-term behavioural responses to a problem-solving task during breeding in a wild population of great tits (Parus major) naturally infected with malaria. Adult females treated against malaria were more active than control females, even though they were not more likely to solve the task or learn how to do so, suggesting that energetic constraints could shape differences in some behaviours while changes in cognitive performances might require more time for the neural system to recover or may depend mainly on infection at the developmental stage. Alternatively, parasite load might be a consequence, rather than a cause, of inter-individual variation in cognitive performance. These results also suggest that inter-individual as well as inter-population differences in some behavioural traits may be linked to blood parasite load.

Multivariate selection and intersexual genetic constraints in a wild bird population.

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra- and intersex additive genetic (co)variances and sex-specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex-specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex-specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross-sex genetic correlation=-0.003, 95% CI=-0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex-specific effects, was estimated at 50% (95% CI=13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.

No evidence for MHC class I‐based disassortative mating in a wild population of great tits

Genes of the major histocompatibility complex (MHC) are regarded as a potentially important target of mate choice due to the fitness benefits that may be conferred to the offspring. According to the complementary genes hypothesis, females mate with MHC dissimilar males to enhance the immunocompetence of their offspring or to avoid inbreeding depression. Here, we investigate whether selection favours a preference for maximally dissimilar or optimally dissimilar MHC class I types, based on MHC genotypes, average amino acid distances and the functional properties of the antigen-binding sites (MHC supertypes); and whether MHC type dissimilarity predicts relatedness between mates in a wild great tit population. In particular, we explore the role that MHC class I plays in female mate choice decisions while controlling for relatedness and spatial population structure, and examine the reproductive fitness consequences of MHC compatibility between mates. We find no evidence for the hypotheses that females select mates on the basis of either maximal or optimal MHC class I dissimilarity. A weak correlation between MHC supertype sharing and relatedness suggests that MHC dissimilarity at functional variants may not provide an effective index of relatedness. Moreover, the reproductive success of pairs did not vary with MHC dissimilarity. Our results provide no support for the suggestion that selection favours, or that mate choice realizes, a preference for complimentary MHC types.

Genetic background, and not ontogenetic effects, affects avian seasonal timing of reproduction

Avian seasonal timing is a life-history trait with important fitness consequences and which is currently under directional selection due to climate change. To predict micro-evolution in this trait, it is crucial to properly estimate its heritability. Heritabilities are often estimated from pedigreed wild populations. As these are observational data, it leaves the possibility that the resemblance between related individuals is not due to shared genes but to ontogenetic effects; when the environment for the offspring provided by early laying pairs differs from that by late pairs and the laying dates of these offspring when they reproduce themselves is affected by this environment, this may lead to inflated heritability estimates. Using simulation studies, we first tested whether and how much such an early environmental effect can inflate heritability estimates from animal models, and we showed that pedigree structure determines by how much early environmental effects inflate heritability estimates. We then used data from a wild population of great tits (Parus major) to compare laying dates of females born early in the season in first broods and from sisters born much later, in second broods. These birds are raised under very different environmental conditions but have the same genetic background. The laying dates of first and second brood offspring do not differ when they reproduce themselves, clearly showing that ontogenetic effects are very small and hence, family resemblance in timing is due to genes. This finding is essential for the interpretation of the heritabilities reported from wild populations and for predicting micro-evolution in response to climate change.

Explaining variance of avian malaria infection in the wild: the importance of host density, habitat, individual life-history and oxidative stress

BackgroundAvian malaria (Plasmodium sp.) is globally widespread, but considerable variation exists in infection (presence/absence) patterns at small spatial scales. This variation can be driven by variation in ecology, demography, and phenotypic characters, in particular those that influence the host’s resistance. Generation of reactive oxygen species (ROS) is one of the host’s initial immune responses to combat parasitic invasion. However, long-term ROS exposure can harm the host and the redox response therefore needs to be adjusted according to infection stage and host phenotype. Here we use experimental and correlational approaches to assess the relative importance of host density, habitat composition, individual level variation and redox physiology for Plasmodium infection in a wild population of great tits, Parus major.ResultsWe found that 36% of the great tit population was infected with Plasmodium (22% P. relictum and 15% P. circumflexum prevalence) and that patterns of infection were Plasmodium species-specific. First, the infection of P. circumflexum was significantly higher in areas with experimental increased host density, whereas variation in P. relictum infection was mainly attributed to age, sex and reproduction. Second, great tit antioxidant responses – total and oxidizied glutathione - showed age- , sex- and Plasmodium species-specific patterns between infected and uninfected individuals, but reactive oxygen metabolites (ROM) showed only a weak explanatory power for patterns of P. relictum infection. Instead ROM significantly increased with Plasmodium parasitaemia.ConclusionsThese results identify some key factors that influence Plasmodium infection in wild birds, and provide a potential explanation for the underlying physiological basis of recently documented negative effects of chronic avian malaria on survival and reproductive success.

Individual and Population-Level Impacts of an Emerging Poxvirus Disease in a Wild Population of Great Tits

Emerging infectious diseases of wildlife can have severe effects on host populations and constitute a pressing problem for biodiversity conservation. Paridae pox is an unusually severe form of avipoxvirus infection that has recently been identified as an emerging infectious disease particularly affecting an abundant songbird, the great tit (Parus major), in Great Britain. In this study, we study the invasion and establishment of Paridae pox in a long-term monitored population of wild great tits to (i) quantify the impact of this novel pathogen on host fitness and (ii) determine the potential threat it poses to population persistence. We show that Paridae pox significantly reduces the reproductive output of great tits by reducing the ability of parents to fledge young successfully and rear those young to independence. Our results also suggested that pathogen transmission from diseased parents to their offspring was possible, and that disease entails severe mortality costs for affected chicks. Application of multistate mark-recapture modelling showed that Paridae pox causes significant reductions to host survival, with particularly large effects observed for juvenile survival. Using an age-structured population model, we demonstrate that Paridae pox has the potential to reduce population growth rate, primarily through negative impacts on host survival rates. However, at currently observed prevalence, significant disease-induced population decline seems unlikely, although pox prevalence may be underestimated if capture probability of diseased individuals is low. Despite this, because pox-affected model populations exhibited lower average growth rates, this emerging infectious disease has the potential to reduce the resilience of populations to other environmental factors that reduce population size.

Problem-solving performance is correlated with reproductive success in a wild bird population

Although interindividual variation in problem-solving ability is well documented, its relation to variation in fitness in the wild remains unclear. We investigated the relationship between performance on a problem-solving task and measures of reproductive success in a wild population of great tits, Parus major. We presented breeding pairs during the nestling provisioning period with a novel string-pulling task requiring the parents to remove an obstacle with their leg that temporarily blocked access to their nestbox. We found that nests where at least one parent solved the task had higher nestling survival until fledging than nests where both parents were nonsolvers. Furthermore, clutch size, hatching success and fledgling number were positively correlated with speed in solving the task. Our study suggests that natural selection may directly act on interindividual variation in problem-solving performance. In light of these results, the mechanisms maintaining between-individual variation in problem-solving performance in natural populations need further investigation.

Activity Patterns during Food Provisioning Are Affected by Artificial Light in Free Living Great Tits (Parus major)

Artificial light may have severe ecological consequences but there is limited experimental work to assess these consequences. We carried out an experimental study on a wild population of great tits (Parus major) to assess the impact of light pollution on daily activity patterns during the chick provisioning period. Pairs that were provided with a small light outside their nest box did not alter the onset, cessation or duration of their working day. There was however a clear effect of artificial light on the feeding rate in the second half of the nestling period: when provided with artificial light females increased their feeding rate when the nestlings were between 9 and 16 days old. Artificial light is hypothesised to have affected the perceived photoperiod of either the parents or the offspring which in turn led to increased parental care. This may have negative fitness consequences for the parents, and light pollution may thus create an ecological trap for breeding birds.

Exploration behaviour is not associated with chick provisioning in great tits.

In biparental systems, members of the same pair can vary substantially in the amount of parental care they provide to offspring. The extent of this asymmetry should depend on the relative costs and benefits of care. Individual variation in personality is likely to influence this trade-off, and hence is a promising candidate to explain differences in care. In addition, plasticity in parental care may also be associated with personality differences. Using exploration behaviour (EB) as a measure of personality, we investigated these possibilities using both natural and experimental data from a wild population of great tits (Parus major). Contrary to predictions, we found no association between EB and natural variation in provisioning behaviour. Nor was EB linked to responsiveness to experimentally increased brood demand. These results are initially surprising given substantial data from other studies suggesting personality should influence investment in parental care. However, they are consistent with a recent study showing selection on EB is weak and highly context-specific in the focal population. This emphasises the difficulty faced by personality studies attempting to make predictions based on previous work, given that personalities often vary among populations of the same species.

Speeding Up Microevolution: The Effects of Increasing Temperature on Selection and Genetic Variance in a Wild Bird Population

Author SummaryThe speed of evolutionary change in a phenotypic trait is determined by two key components: the amount of genetic variance underlying the trait and the strength of selection acting on it. Many studies have shown that both selection and expression of genetic variance may depend on the environmental conditions the population experiences. However, the possibility that the strength of selection and the expression of genetic variance become positively or negatively associated as a result of this environmental covariance, so as to speed up or hamper an evolutionary response, has been largely ignored. Here we show that, in a wild bird population, the annual strength of selection on and the expression of genetic variance in timing of breeding (a key life history trait) are positively associated due to changing environmental conditions (warmer temperatures). Such a positive association should potentially speed up any microevolutionary response to selection (such as that imposed by climate warming). Our results illustrate the existence of substantial temporal variation in response to environmental heterogeneity, and thus highlight a so far neglected mechanism that may be important in determining the evolutionary dynamics in natural populations.

SPATIAL SCALE OF LOCAL BREEDING HABITAT QUALITY AND ADJUSTMENT OF BREEDING DECISIONS

Experimental studies provide evidence that, in spatially and temporally heterogeneous environments, individuals track variation in breeding habitat quality to adjust breeding decisions to local conditions. However, most experiments consider environmental variation at one spatial scale only, while the ability to detect the influence of a factor depends on the scale of analysis. We show that different breeding decisions by adults are based on information about habitat quality at different spatial scales. We manipulated (increased or decreased) local breeding habitat quality through food availability and parasite prevalence at a small (territory) and a large (patch) scale simultaneously in a wild population of Great Tits (Parus major). Females laid earlier in high-quality large-scale patches, but laying date did not depend on small-scale territory quality. Conversely, offspring sex ratio was higher (i.e., biased toward males) in high-quality, small-scale territories but did not depend on large-scale patch quality. Clutch size and territory occupancy probability did not depend on our experimental manipulation of habitat quality, but territories located at the edge of patches were more likely to be occupied than central territories. These results suggest that integrating different decisions taken by breeders according to environmental variation at different spatial scales is required to understand patterns of breeding strategy adjustment.