Population Of Great Tits Research Articles

Consistent individual differences in the social phenotypes of wild great tits, Parus major

Despite growing interest in animal social networks, surprisingly little is known about whether individuals are consistent in their social network characteristics. Networks are rarely repeatedly sampled; yet an assumption of individual consistency in social behaviour is often made when drawing conclusions about the consequences of social processes and structure. A characterization of such social phenotypes is therefore vital to understanding the significance of social network structure for individual fitness outcomes, and for understanding the evolution and ecology of individual variation in social behaviour more broadly. Here, we measured foraging associations over three winters in a large PIT-tagged population of great tits, and used a range of social network metrics to quantify individual variation in social behaviour. We then examined repeatability in social behaviour over both short (week to week) and long (year to year) timescales, and investigated variation in repeatability across age and sex classes. Social behaviours were significantly repeatable across all timescales, with the highest repeatability observed in group size choice and unweighted degree, a measure of gregariousness. By conducting randomizations to control for the spatial and temporal distribution of individuals, we further show that differences in social phenotypes were not solely explained by within-population variation in local densities, but also reflected fine-scale variation in social decision making. Our results provide rare evidence of stable social phenotypes in a wild population of animals. Such stable social phenotypes can be targets of selection and may have important fitness consequences, both for individuals and for their social-foraging associates.

Estimating the variation, autocorrelation, and environmental sensitivity of phenotypic selection

Despite considerable interest in temporal and spatial variation of phenotypic selection, very few methods allow quantifying this variation while correctly accounting for the error variance of each individual estimate. Furthermore, the available methods do not estimate the autocorrelation of phenotypic selection, which is a major determinant of eco-evolutionary dynamics in changing environments. We introduce a new method for measuring variable phenotypic selection using random regression. We rely on model selection to assess the support for stabilizing selection, and for a moving optimum that may include a trend plus (possibly autocorrelated) fluctuations. The environmental sensitivity of selection also can be estimated by including an environmental covariate. After testing our method on extensive simulations, we apply it to breeding time in a great tit population in the Netherlands. Our analysis finds support for an optimum that is well predicted by spring temperature, and occurs about 33 days before a peak in food biomass, consistent with what is known from the biology of this species. We also detect autocorrelated fluctuations in the optimum, beyond those caused by temperature and the food peak. Because our approach directly estimates parameters that appear in theoretical models, it should be particularly useful for predicting eco-evolutionary responses to environmental change.

Differential Effects of Maternal Yolk Androgens on Male and Female Offspring: A Role for Sex-Specific Selection?

Maternal hormones are important mediators of prenatal maternal effects in animals. Although their effects on offspring phenotype are often sex-specific, the reason why sometimes sons are more sensitive to prenatal hormone exposure and sometimes daughters is not well understood. Here I combine an experimental manipulation of yolk testosterone concentration in the egg and quantification of selection acting on yolk androgen-sensitive traits in a natural population of great tits (Parus major) with a literature review to test the hypothesis that sex-specific selection on traits affected by yolk androgens determines which sex is more sensitive to prenatal hormone exposure. An experimental increase of the testosterone content in the egg boosted the post-hatching growth of male, but not female great tit nestlings. However, I found no evidence that survival selection on body mass or size is acting differently in the two sexes. A literature review revealed that yolk androgen manipulations affect the growth of males and females differently across species. Interestingly, in studies performed in the wild a significant association between the strength and direction of sexual size dimorphism and sex-specific sensitivities to yolk androgens was observed. In studies performed in captivity, no such relationship was found. Thus, across species there is some evidence that sex-specific selection on body size influences how strongly growth trajectories of males and females are affected by maternally-derived yolk androgens.

Reproductive consequences of the timing of seasonal movements in a nonmigratory wild bird population

Animal movement patterns, whether related to dispersal, migration, or ranging behaviors, vary in time. Individual movements reflect the outcomes of interactions between an individual's condition and a multitude of underlying ecological processes. Theory predicts that when competition for breeding territories is high, individuals should arrive at breeding sites earlier than what would otherwise be optimal for breeding in the absence of competition. This is because priority at a site can confer significant competitive advantages leading to better breeding outcomes. Empirical data from long‐distance migrants support this theory. However, it has not been tested within the context of fine‐scale movements in nonmigratory populations. We assessed the effect of arrival time at a breeding site on reproductive outcomes in an intensively monitored resident population of Great Tits (Parus major). The population was monitored passively, via passive integrated transponder (PIT) tag loggers, and actively, via catching, during breeding and nonbreeding seasons. We developed new capture–recapture–resight models that use both data types to model breeding outcome conditional on the unknown individual arrival times. In accordance with theory, individuals arrived at the woods synchronously in waves that were large at the beginning of the nonbreeding season and small toward the end, with very few arrivals in the intervening period. There was a strong effect of arrival time on the probability of breeding; the earlier an individual arrived, the more likely it was to successfully establish a nest that reached the incubation period. However, once nests were established, they had equal probabilities of failing early, regardless of arrival time. Finally, there was moderate evidence of a negative effect of arrival time on the probability of successfully fledging nestlings. These empirical findings are consistent with theoretical models that suggest an important role for competition in shaping fine‐scale seasonal movements. Our capture–recapture–resight models are extensible and suitable for a variety of applications, particularly when the goal is to estimate the effects of unobservable arrival times on subsequent ecological outcomes.

Evidence of a link between survival and pair fidelity across multiple tit populations

Although they have the potential to strongly influence individual fitness and the dynamics and productivity of populations, the survival consequences of pairing outcomes and the influence of current pairing outcomes on those in the future have rarely been addressed. Previously, we have shown that pair fidelity increases both survival and future pair fidelity in a population of great titsParus major. The aim of this study was to explore the generality of our previous findings by evaluating the influence of current paring outcomes on survival and on future pairing outcomes in two different species and in different populations. We addressed our aims within a multievent capture–mark–recapture (MECMR) statistical framework, which accounts for differences in recapture rates and uncertainty in the assignment of pair status (i.e. whether an individual is breeding with the same partner or not). We applied the framework to breeding records of two great tit populations and one blue titCyanistes caeruleuspopulation. We detected survival benefits (i.e. increased survival) of pair fidelity in all three populations. These were similar in both great tit populations, but higher for male great tits than for male blue tits. We found that age‐dependence in the rate of pair fidelity was shared between different populations and species, but did not detect any influence of current pair status on future pair status. Our study highlights the importance of considering survival when studying the fitness benefits of pair fidelity. Some of the differences in pair fidelity rates and survival benefits of pair fidelity are likely the result of long‐term and short‐term demographic and environmental factors in the population. We advocate the use of the MECMR framework used here for further exploration of these differences.

Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits

Oxidative stress has been suggested as a mechanism underlying the costs of reproduction and life history trade-offs. Reproductive activities may lead to high production of pro-oxidants, whose activity can generate oxidative damage when not countered by adequate antioxidant defenses. Because inter-individual differences in the efficiency of the antioxidant system are influenced by an individual’s diet, food availability experienced during reproduction may affect the females’ antioxidant status and, in birds, their ability to transfer antioxidants into their eggs. Moreover, a female’s ability to cope with oxidative stress has been suggested to influence pigment deposition in the eggshell, suggesting a possible signaling function of eggshell maculation. Here we performed a food supplementation experiment in a natural population of great tits (Parus major) in order to investigate how nutritional conditions experienced during the egg laying period affect the female’s oxidative status and egg investment and how maternal oxidative status and egg antioxidant protection relate to eggshell pigmentation. We show that food-supplemented females had lower oxidative damage levels (ROMs) than non-food-supplemented females. Furthermore, a female’s ROMs levels were negatively associated with the levels of yolk antioxidant protection in her eggs, but this negative association was only significant in non-food-supplemented females. This suggests that oxidative stress experienced during reproduction influences the allocation of antioxidants into the eggs. Moreover, we observed a positive relationship between eggshell pigment distribution and maternal and yolk antioxidant protection, suggesting that eggshell pigmentation is a cue of female (and offspring) quality.

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.

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.

Physiological responses to increased brood size and ectoparasite infestation: Adult great tits favour self-maintenance

Different types of stressors trigger responses of different physiological systems, and these responses may contribute differentially to the maintenance of homeostasis, to trade-offs and the evolution of life-history traits. To manipulate two common stressors during reproduction, we infested half of the nests in a naturally breeding great tit population with ectoparasites and simultaneously manipulated brood size, using a 2×2 experimental design. Parents in this model species commonly compensate for ectoparasites by an increase in food provisioning. We assessed parental responses to these concurrent stressors by measuring several physiological stress parameters such as changes in metabolic rate, oxidative stress and expression of heat-shock proteins (Hsp), and explored how these stressors affect the trade-off between self-maintenance and reproduction. Neither flea infestation nor brood size manipulation affected adult metabolic rate, oxidative damage or Hsp levels. Furthermore, we found no interactive effect of the two treatments on adults. However, nestlings in infested nests had lower body mass and lower survival. Nestlings in enlarged broods were lighter and had lower survival, although parents of enlarged broods increased food provisioning rate. The findings suggest that adults favour maintenance of cellular homeostasis, and physiological equilibrium over current reproduction, and that the costs induced by both stressors, flea infestation and increased brood size, are carried by the offspring. It emphasizes the importance of self-maintenance over reproduction in life-history decisions, and more generally the need of including physiological traits for understanding the evolution of life-histories.

Different reactions to aposematic prey in 2 geographically distant populations of great tits

Variation in predator behavior toward aposematic prey was frequently studied at interspecific and individual levels, but interpopulation differences have been neglected. Geographic differences in prey fauna offer an opportunity to test their implications for predator behavior. It can be expected that 1) predator populations inhabiting environments with high diversity of aposematic prey are more neophobic than those living in areas where aposematic prey are scarce, and 2) different levels of neophobia jointly with avoidance learning affect selection on aposematic prey. We compared the behavior of wild-caught great tits (Parus major) from Bohemia and Central Finland toward aposematic firebugs (Pyrrhocoris apterus), nonaposematic firebugs, novel objects and novel palatable nonaposematic prey. Finnish and Bohemian birds did not differ in their novel-object exploration, but Finnish birds hesitated longer than Bohemian birds before resuming feeding next to a novel object. Latencies to attack novel palatable prey did not differ and were not correlated with the attitude toward novel objects. Tits from the Bohemian population mostly avoided aposematic firebugs and attacked nonaposematic ones. Finnish birds were more likely to attack both firebug color forms, and their attack latencies were correlated with latencies of attacking novel palatable prey. Thus, Bohemian birds avoided the aposematic prey, but were not more neophobic than Finnish birds. These results suggest that differences between Finnish and Bohemian birds in behavior to aposematic prey do not follow differences in exploration strategy and neophobia. The observed differences can be explained by a different experience with local aposematic prey communities.

No evidence for correlational selection on exploratory behaviour and natal dispersal in the great tit

A growing number of studies have recently reported links between personality and dispersal, yet the adaptive significance of personality-dependent dispersal strategies still remain poorly understood. Here, we tested whether birds differing in exploratory behaviour (EB, quantified by a novel environment test), gain differential fitness benefits when remaining in or leaving their natal area in a natural population of great tits (Parus major). Using data on lifetime fecundity, we found no evidence that particular combinations of EB and dispersal lead to a higher fitness after settlement. In males, we found positive selection acting on EB through first-year survival, resulting in a positive relationship between EB and number of lifetime fledglings. However, contrary to expectation, these effects were only present in local recruits and not in immigrants. Male immigrants produced fewer fledglings during their lifetime than did local recruits, suggesting selection against dispersal at a scale exceeding the size of our study area. In females, we found selection on EB through recruitment with respect to year (i.e., negative, positive and stabilizing selection), but neither the strength nor the direction differed among birds with different dispersal strategies. We found no evidence in either sex for lifetime selection acting on EB using recruits as a measure of fitness. In conclusions, our results do not support the hypothesis that the co-expression of personality and dispersal is shaped by selection after settlement.

Allelic variation at innate immune genes (avian β‐defensins), within a natural population of great tits

In order to fully understand pathogen induced natural variation in fitness in wild animal populations it is important to identify and study the degree of non‐synonymous alleles in genes that code for components of the immune system. This study investigates the degree of natural genetic variation at 6 innate immune genes belonging to the β‐defensin family within a single population of birds, the great tits Parus major. In 40 adult individuals, all belonging to the same local population in Wytham Woods, Oxford, UK, screened across 6 different β‐defensin genes, all but one individual showed non‐synonymous heterozygosity within the exon coding for the mature defensin peptide. The non‐synonomous variation was thus associated with the part of the defensin gene that directly interacts with potential pathogens. Within the sample, 31 different genotypes were identified across the 6 different loci. Much of the found allelic variation affected the amino acid composition, which in turn alter the net charge and hydrophilicity of the produced peptide; properties associated with the efficiency of binding to and rupture pathogens.This study demonstrates that non‐synonymous genetic variation exists at β‐defensins genes, a part of the immune system that forms an important first line of defence against various pathogens. Understanding the degree of underlying genetic variation at different parts of the immune system will help achieve a holistic view of the reasons behind individual variation in pathogen susceptibility, as well as why individuals are affected differently once they become infected.

Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits.

Parasites are known to exert selective pressures on host life history traits since the energy and nutrients needed to mount an immune response are no longer available to invest in other functions. Bird feathers harbour numerous microorganisms, some of which are able to degrade feather keratin (keratinolytic microorganisms) and affect feather integrity and colouration in vitro. Although named "feather-degrading" microorganisms, experimental evidence for their effects on feathers of free-living birds is still lacking. Here, we tested whether (i) keratinolytic microorganisms can degrade feathers in vivo and thus modify the colour of feathers during the nesting period and (ii) whether feather microorganisms have a long-term effect on the investment in colouration of newly moulted feathers. We designed treatments to either favour or inhibit bacterial growth, thus experimentally modifying plumage bacterial communities, in a wild breeding population of great tits (Parus major). Our analyses revealed no significant effects of the treatments on feather colours. Moreover, we found that differences in bacterial exposure during nesting did not significantly affect the colouration of newly moulted feathers. Our results suggest that significant feather degradation obtained during in vitro studies could have led to an overestimation of the potential of keratinolytic microorganisms to shape feather colouration in free-living birds.

Effects of early-life lead exposure on oxidative status and phagocytosis activity in great tits (Parus major)

Lead is a highly poisonous metal with a very long half-life, distributing throughout the body in blood and accumulating primarily in bones and kidney. We studied the short and long-term effects of early-life lead exposure on antioxidant defense and phagocytosis activity in a small passerine bird, the great tit (Parus major) by manipulating dietary lead levels of the nestlings. We had three experimental groups, exposed to environmentally relevant lead concentrations; high (4μg/g body mass), low (1μg/g body mass) and control (0μg/g body mass) group. As a comparison, a great tit population breeding in the vicinity of a metal smelter was included to the experimental set-up. We measured glutathione, the ratio of reduced and oxidized glutathione, and the antioxidant enzymes: glutathione peroxidase, glutathione-S-transferase, catalase and superoxide dismutase together with protein carbonylation and phagocytosis activity to study the effects of lead on the oxidative status and immune function of birds. We found differences in enzyme activities between the study groups, but in most cases the smelter group differed from the other groups. Despite the differences observed in antioxidant enzymes, our results indicate only minor short-term effects of lead exposure on oxidative status, since either glutathione ratio or protein carbonylation were not affected by lead. Phagocytosis activity was not linked to higher lead concentrations either. Interestingly, protein carbonylation was positively associated with enzyme activities and glutathione level. Our results did not show major long-term effects of lead on the oxidative status of great tits.

Розмір кладки та успішність розмноження синиці великої (Parus major) та блакитної (P. caeruleus) у парках м. Харків

Установлено середній розмір повної кладки синиці великої 8,9 ± 0,35 (n = 61) та синиці блакитної 9,5 ± 0,33 (n = 12). У синиці великої більшу частину складають 10- (33,5%) та 9-яйцеві (16,7%) кладки. У синиці блакитної переважають 10-яйцеві (25,0%) кладки у Журавлівському гідропарку та 12-яйцеві (17,5%) – у парку імені М. Горького. Встановлено високу успішність розмноження у синиці великої (85,1%) та блакитної (84,0%). У середньому на одну пару синиці великої із гнізда злітає 5,1 ± 0,16 пташеняти, у синиці блакитної – 8,5 ± 0,38 пташеняти. Це свідчить про стабільність урбопопуляції. Протягом існування популяції у синиці великої виявлено залежність зменшення успішності розмноження: у Журавлівському гідропарку у рік розміщення штучних гніздівель із гнізд злетіло у середньому 6,7 ± 0,12 пташеняти на одну пару, упродовж чотирьох років ця величина зменшилась майже удвічі і становила 3,6 ± 0,15. У синиці блакитної такої залежності не виявлено. Найпродуктивнішими у синиці великої виявилися кладки третьої декади квітня (89,7%), що у середньому складає 8,9 ± 0,78 пташеняти на одну пару. Найуспішнішими є 10-яйцеві кладки, частка зльоту пташенят із яких становила 98,3%, що у середньому складає 9,8 ± 0,18 на одну пару.

Incubation and hatching periods in a Mediterranean Great Tit Parus major population

Capsule The onset of incubation relative to clutch completion is highly variable in Great Tits Parus major, and has important consequences for the duration of the incubation and hatching periods.Aim To investigate when incubation starts relative to clutch completion, its effects on the length of the incubation and hatching periods, and which proximate factors affect all of these traits.Methods We used data from a Great Tit population in Eastern Spain collected over 15 years. Periodic visits to the nests (daily at some stages) allowed the determination of breeding parameters of interest. General linear models were used for analyses.Results On average, incubation started the day of laying of the last egg and lasted 13.2 days. The hatching period lasted 1.7 days. Incubation started earlier relative to clutch completion as temperatures during the laying period were higher and as clutch size increased. The incubation period was shorter if incubation started later relative to clutch completion. Hatching asynchrony increased as incubation started earlier relative to clutch completion and as the incubation period decreased.Conclusions The onset of incubation relative to clutch completion is highly variable, and has important consequences for the duration of the incubation and hatching periods. Starting incubation before or after clutch completion could, respectively, advance or delay the hatching date, although advancement would be at the cost of increasing the degree of hatching asynchrony.

Are colorful males of great tits Parus major better parents? Parental investment is a matter of quality

Given the known influence of parental investment on breeding success of great tits Parus major, females should be expected to use male parental quality as an essential criterion in mate choice. Since parental quality cannot usually be observed directly at the time of pairing, it has been suggested that females rely on male ornaments as indicative of their ability to provide parental care. This hypothesis, called the good parent hypothesis, has been tested repeatedly assessing only parental effort as the number of feedings made by parents. However, in evaluating parental investment, the focus should also be on the quality of prey captured rather than only on its quantity. We analyzed feeding rates and the provisioning of different prey in relation to both male yellow carotenoid-based breast coloration and the size of the black melanin-based stripe in a Mediterranean great tit population. We predicted that more carotenoid ornamented individuals would feed nestlings with a diet consisting of a higher proportion of caterpillars. However, and contrary to predictions, we found that males with higher values of hue in the yellow breast feathers, fed their offspring with a lower proportion of caterpillars and a higher proportion of spiders. In addition, nestlings that received a higher proportion of spiders showed an improved body condition after controlling for tarsus length and other variables. Male feeding rates correlated positively with brood size and tended to correlate negatively with date, although we did not find any effect of male coloration. Our data therefore support the good parent hypothesis, insofar as parental investment is also a matter of quality, and that, at least in the Mediterranean area, caterpillars are not the only key food source.

Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates.

Linking variation in quantitative traits to variation in the genome is an important, but challenging task in the study of life-history evolution. Linkage maps provide a valuable tool for the unravelling of such trait−gene associations. Moreover, they give insight into recombination landscapes and between-species karyotype evolution. Here we used genotype data, generated from a 10k single-nucleotide polymorphism (SNP) chip, of over 2000 individuals to produce high-density linkage maps of the great tit (Parus major), a passerine bird that serves as a model species for ecological and evolutionary questions. We created independent maps from two distinct populations: a captive F2-cross from The Netherlands (NL) and a wild population from the United Kingdom (UK). The two maps contained 6554 SNPs in 32 linkage groups, spanning 2010 cM and 1917 cM for the NL and UK populations, respectively, and were similar in size and marker order. Subtle levels of heterochiasmy within and between chromosomes were remarkably consistent between the populations, suggesting that the local departures from sex-equal recombination rates have evolved. This key and surprising result would have been impossible to detect if only one population was mapped. A comparison with zebra finch Taeniopygia guttata, chicken Gallus gallus and the green anole lizard Anolis carolinensis genomes provided further insight into the evolution of avian karyotypes.

Heritability of gonad size varies across season in a wild songbird

Many organisms advance their seasonal reproduction in response to global warming. In birds, which regress their gonads to a nonfunctional state each winter, these shifts are ultimately constrained by the time required for gonadal development in spring. Gonadal development is photoperiodically controlled and shows limited phenotypic plasticity in relation to environmental factors, such as temperature. Heritable variation in the time required for full gonadal maturation to be completed, based on both onset and speed of development and resulting in seasonally different gonad sizes among individuals, is thus a crucial prerequisite for an adaptive advancement of seasonal reproduction in response to changing temperatures. We measured seasonal gonadal development in climate-controlled aviaries for 144 great tit (Parus major) pairs, which consisted of siblings obtained as whole broods from the wild. We show that the extent of ovarian follicle development (follicle size) in early spring is highly heritable (h(2) = 0.73) in females, but found no heritability of the extent of testis development in males. However, heritability in females decreased as spring advanced, caused by an increase in environmental variance and a decrease in additive genetic variation. This low heritability of the variation in a physiological mechanism underlying reproductive timing at the time of selection may hamper genetic adaptation to climate change, a key insight as this great tit population is currently under directional selection for advanced egg-laying.

Exploring patterns of variation in clutch size–density reaction norms in a wild passerine bird

Negative density dependence of clutch size is a ubiquitous characteristic of avian populations and is partly due to within-individual phenotypic plasticity. Yet, very little is known about the extent to which individuals differ in their degree of phenotypic plasticity, whether such variation has a genetic basis and whether level of plasticity can thus evolve in response to selection. Using 18years of data of a Dutch great tit population (Parus major), we show that females reduced clutch size with increasing population density (slopes of the reaction norms), differed strongly in their average clutch size (elevations of the reaction norms) at the population-mean density and that the latter variation was partly heritable. In contrast, we could not detect individual variation in phenotypic plasticity ('I×E'). Level of plasticity is thus not likely to evolve in response to selection in this population. Observed clutch sizes deviated more from the estimated individual reaction norms in certain years and densities, implying that the within-individual between-year variance (so-called residual variance) of clutch size was heterogeneous with respect to these factors. Given the observational nature of this study, experimental manipulation of density is now warranted to confirm the causality of the observed density effects. Our analyses demonstrate that failure to acknowledge this heterogeneity would have inflated the estimate of 'I×E' and led to misinterpretation of the data. This paper thereby emphasizes the fact that heterogeneity in residuals can provide biologically insightful information about the ecological processes underlying the data.