Individual variation in behaviour

Wild animals show remarkable phenotypic variation despite natural selection eroding it. Phenotypic variation within populations is intriguing because all individuals are expected to be adapted to the same environmental conditions, and thus, to present similar phenotypic traits. However, when repeatedly measured, individuals have been observed to differ in the average expression of various behaviours across time and contexts. Consistent among-individual variation (called “animal personality”) has been proposed to be adaptively maintained if the fitness costs and benefits of behaviour vary with the environment or other phenotypic traits. Theory postulates that two key adaptive mechanisms could play a role: life-history trade-offs and spatiotemporal variation in selection (or heterogeneous selection). Empirical tests of the role of these mechanisms in the maintenance of individual variation in behaviour remain scarce and findings are ambivalent. My PhD thesis aimed at shedding light on the mechanisms allowing the persistence of animal personalities, thereby advancing our understanding of how animals adapt to variable environments. I investigated the role of life-history trade-offs and heterogeneous selection in the coexistence of alternative personalities in the wild. I also examined potential ecological drivers of heterogeneous selection. I used a passerine bird breeding in the wild in nest boxes (the great tit Parus major) as model. Individuals must trade-off investment among various phenotypic traits because they have limited amount of energy and time to acquire resources, grow and reproduce. The optimal resolution of trade-offs may depend on ecological conditions and/or the phenotypic traits of the individuals. Individuals differing in their behavioural phenotypes may thus resolve trade-offs differently. In Chapter 1, my colleagues and I tested this hypothesis by focusing on the trade-off between current reproduction and reproductive senescence. Specifically, we asked whether behavioural phenotypes differed in patterns of senescence. We found that faster explorers increased and subsequently decreased their reproductive investment with age. This finding suggests that faster explorers reproductively senesced later in life. By contrast, slower explorers laid similar clutch sizes through their lifetime; that is, they did not show reproductive senescence. Different behavioural phenotypes, thus, resolved the trade-off between current reproduction and reproductive senescence differently, which may allow them to coexist. Spatial and temporal variation in the environment may cause natural selection to favour different phenotypes in different environments. Spatial variation in selection may maintain phenotypic variation across environments, whereas temporal variation in selection (or fluctuating selection) may maintain phenotypic variation within environments. Though these processes co-occur and may have counteracting effects on phenotypic variation, both processes have rarely been investigated simultaneously. The relative importance of spatial and temporal variation in selection, and thus, the evolutionary potential of phenotypic traits under heterogeneous selection, remains unexplored. In Chapter 2, I studied heterogeneous selection on behaviour within and among great tit populations. To this aim, I gathered longitudinal data from five West European wild great tit populations breeding in nest boxes. In all these populations, behaviour was assayed with the same experimental design. Selection on behaviour varied primarily spatially. Temporal variation in selection was also important. The existence of phenotypic variation in all populations suggests that temporal variation played a key role in counteracting local adaption promoted by spatial variation. Temporal variation in selection was population-specific, which suggests that local ecological conditions also played a role in the evolution of phenotypic variation. This study thereby demonstrated the importance of considering both large- and small-scale geographical and temporal variation to understand the ecological mechanisms maintaining variation in animal behaviour. Previous studies found that variation in the social environment induced by variation in population density caused selection on behaviour to vary. However, we did not find such evidence in great tit populations. Another ecological factor that varies ubiquitously and that is crucial for survival and reproduction is food availability. Food availability also generally positively correlates with population density. Therefore, the effects of population density on fitness may be indirect through food availability. Variation in food availability may cause selection pressures on behaviour to vary because behavioural phenotypes differ in competitive abilities and foraging tactics. In Chapter 3, I studied whether winter food availability drove heterogeneous selection on activity in a novel environment. I experimentally manipulated food abundance outside the breeding season by providing supplementary food in multiple great tit nest box plots. Against expectations, I did not find evidence for fecundity selection on behaviour to vary with the experimental manipulation of food availability. Food availability may drive variation in fecundity selection but simultaneous changes in breeding density may counteract its action. Food- and density-dependent selection on behaviour need to be estimated simultaneously to disentangle their effects. Interestingly, on average, individuals were more active in high than in low food availability context. Moreover, high food availability context increased behavioural variation among individuals. These findings suggest greater plasticity and/or higher survival, recruitment or immigration rate of more active individuals. Future studies should investigate whether viability rather than fecundity selection vary with food availability. In the different projects of this PhD work, I focused on behaviour scored in different “novel environments”, which are all generally labelled “exploration behaviour”. However, “exploration behaviour” was not assayed with the same experimental design in Chapter 2 compared to Chapter 1 and 3. In Chapter 1 and 3, behaviour was assayed in the field in a portable cage. In Chapter 2, behaviour was assayed in a standardized laboratory room. We assumed that birds expressed the same behaviour in both assays because laboratory- and field-based behaviours have been shown to each correlate with other field-based behaviours. In Chapter 4, I tested this assumption and found that laboratory- and field-based behaviour did not correlate. Both assays may present different contexts to the birds, which elicited the expression of different behaviours. I also showed that the population sampled for the laboratory test was biased toward fast explorers. This study highlights the difficulty assaying behaviour in an unbiased and reproducible manner. It is therefore important to cross-validate behavioural assays before making biological assumptions. Overall, this PhD thesis contributed to understanding the role of adaptive mechanisms in individual variation in behaviour and their ecological drivers. This work showed that behavioural phenotypes contribute differently to population dynamics and should thus be considered in ecological and evolutionary studies. This work also exemplified the importance of long-term and collaborative projects. For a comprehensive understanding of phenotypic variation, the next challenge would be to simultaneously consider multiple traits, ecological factors and species that all interact through eco-evolutionary dynamics. Such integrative studies will embrace the complexity of ecological interactions and allow us to better understand how populations adapt to variable environments

Are animal personality, body condition, physiology and structural size integrated? A comparison of species, populations and sexes, and the value of study replication

A major question in behavioural ecology is why behaviour, physiology and morphology are often integrated into syndromes. In great tits, Parus major, for example, explorative males are larger (vs. smaller) and leaner (vs. heavier) compared to less explorative individuals. Unfortunately, considerable debate exists on whether patterns found in specific studies are replicable. This debate calls for study replication among species, populations and sexes. We measured behavioural (exploration), physiological (breathing rate) and morphological traits (body mass, tarsus length, wing length, bill length) in two species (great vs. blue tits Cyanistes caeruleus), two populations (Forstenrieder Park vs. Starnberg) and two sexes (males vs. females). We then tested whether the same pattern of integration characterized all unique combinations of these three biological categories (hereafter called datasets). We used a multi-year repeated measures set-up to estimate among-individual trait correlation matrices for each dataset. We then used structural equation modelling to test for size-dependent behaviour and physiology, size-corrected (i.e. size-independent) behaviour-physiology correlations and size-corrected body mass-dependent behaviour and physiology. Finally, we used meta-analyses to test which structural paths were generally (vs. conditionally) supported (vs. unsupported). We found general and consistent support for size-dependent physiology and size-corrected body mass-dependent physiology across datasets: faster breathers were smaller but heavier for their size. Unexpectedly, condition-dependent behaviour was not supported: explorative birds were neither leaner, nor was this relationship heterogeneous across datasets. All other hypothesized patterns were dataset-specific: the covariance between size and behaviour, and between behaviour and physiology differed in sign between datasets, and both were, on average, not supported. This heterogeneity was not explained by any of our moderators: species, population or sex. The specific pattern of size- and condition-dependent physiology reported for a unique combination of species, population, and sex, thus generally predicted those in others. Patterns of size- or condition-dependent behaviour (i.e. ‘personality’), or behaviour-physiology syndromes reported in specific datasets, by contrast, did not. These findings call for studies revealing the ecological background of this variation and highlight the value of study replication to help understand whether patterns of phenotypic integration reported in one study can be generalized

Table Environment

The table contains data of the quantified environmental factors. Temperature, humidity and light are averaged per daily time interval between 22h00 and 04h00 and noise was averaged over 24 hour time interval

Data from: Multidimensional environmental predictors of variation in avian forest and city life histories

Optimal life-history decisions are shaped by prevailing environmental conditions. In the context of urbanization, environmental differences between urban and rural areas are known to vary across a multitude of axes. The relative roles of specific axes and whether they explain variation in avian life histories between forest and city populations have not often been studied empirically. This study comprehensively views urbanization from a multidimensional environmental perspective. For each of 13 nest box plots of a common passerine bird (the great tit Parus major), we quantified temperature, humidity, light, and noise, and subsequently assessed direct versus indirect effects of each environmental axis on components of annual reproductive success by applying a path analytical framework. All quantified environmental axes, and life-history traits, showed substantial repeatable variation between the plots. Forest and city plots differed tremendously in temperature, humidity, and light. We were able to attribute among-population variation in life history to variation in these environmental effects. However, the simple dichotomy between forest and city populations explained the data best. Birds in the city laid earlier, which indirectly resulted in smaller clutches, and their offspring fledged in poorer condition, compared to conspecifics in forests. Those differences persisted after controlling for temperature, humidity, light, and noise, which implies that they were shaped by other factors than the ones quantified in this study. In summary, our findings question the common interpretation that differences between forest and city areas relate to specific environmental axes that covary with urbanization, especially in in lieu of quantitative measurements

Table Path analysis

The table contains averaged data of life history traits (lay date, clutch size, number fledglings and nestling mass) as well as the quantified environmental factors (humidity, temperature, light and noise) per female (Bird ID) and Year. Averaged data for lay date and clutch size on plot level were used to calculate indirect effects of the path models

Immediate and carry-over effects of perceived predation risk on communication behavior in wild birds

Predation induces strong selection on phenotypic traits, affecting prey via consumptive and nonconsumptive effects. Communication is important for territorial behavior, but can increase susceptibility to predators. Therefore, predation risk should influence prey communication patterns, territoriality, and fitness. We evaluated how this trade-off is resolved via 2 manipulations of perceived predation risk using audio playback in wild great tits (Parus major). In the first experiment, we examined the immediate response of individuals to playback; the second experiment, replicated across 2 years, examined both immediate and carry-over effects (over days) of playback broadcast for a 5-month period (March–July) in 12 nest box populations. Birds exposed to predator sounds showed decreased singing and increased alarming compared to controls, both immediately and on days without play back exposure (carry-over effects). Perceived predation risk did not affect how birds responded to simulated territory intrusions. In combination, these studies’ findings imply that individuals perceive predator vocalizations as “risky” up to days after exposure to predator cues, and adjust their behavior to minimize this risk. However, the lack of effects on territorial aggression implies that individuals are able to weigh the costs of predation against the benefits of each type of vocal behavior. Acknowledging that context changes the relative costs and benefits of antipredator behavior has important consequences for understanding predator–prey dynamics

Moiron et al_Dataset State and Behaviour Integration MS

Moiron et al_Dataset State and Behaviour Integration M

Are animal personality, body condition, physiology and structural size integrated? A comparison of species, populations and sexes, and the value of study replication

Gaona-Gordillo I, Holtmann B, Mouchet A, Hutfluss A, Sanchez-Tojar A, Dingemanse NJ. Are animal personality, body condition, physiology and structural size integrated? A comparison of species, populations and sexes, and the value of study replication. Journal of Animal Ecology. 2023.A major question in behavioural ecology is why behaviour, physiology and morphology are often integrated into syndromes. In great tits, Parus major, for example, explorative males are larger (vs. smaller) and leaner (vs. heavier) compared to less explorative individuals. Unfortunately, considerable debate exists on whether patterns found in specific studies are replicable. This debate calls for study replication among species, populations and sexes.We measured behavioural (exploration), physiological (breathing rate) and morphological traits (body mass, tarsus length, wing length, bill length) in two species (great vs. blue tits Cyanistes caeruleus), two populations (Forstenrieder Park vs. Starnberg) and two sexes (males vs. females). We then tested whether the same pattern of integration characterized all unique combinations of these three biological categories (hereafter called datasets).We used a multi-year repeated measures set-up to estimate among-individual trait correlation matrices for each dataset. We then used structural equation modelling to test for size-dependent behaviour and physiology, size-corrected (i.e. size-independent) behaviour-physiology correlations and size-corrected body mass-dependent behaviour and physiology. Finally, we used meta-analyses to test which structural paths were generally (vs. conditionally) supported (vs. unsupported).We found general and consistent support for size-dependent physiology and size-corrected body mass-dependent physiology across datasets: faster breathers were smaller but heavier for their size. Unexpectedly, condition-dependent behaviour was not supported: explorative birds were neither leaner, nor was this relationship heterogeneous across datasets. All other hypothesized patterns were dataset-specific: the covariance between size and behaviour, and between behaviour and physiology differed in sign between datasets, and both were, on average, not supported. This heterogeneity was not explained by any of our moderators: species, population or sex.The specific pattern of size- and condition-dependent physiology reported for a unique combination of species, population, and sex, thus generally predicted those in others. Patterns of size- or condition-dependent behaviour (i.e. 'personality'), or behaviour-physiology syndromes reported in specific datasets, by contrast, did not. These findings call for studies revealing the ecological background of this variation and highlight the value of study replication to help understand whether patterns of phenotypic integration reported in one study can be generalized

Data from: Functional relations between body mass and risk-taking behavior in wild great tits

Natural selection often favors particular combinations of functionally-related traits, resulting in adaptive phenotypic integration. Phenotypic integration has been proposed as a potential mechanism explaining the existence of repeatable among-individual differences in behavior (i.e., animal personality). In this study, we investigated patterns of covariation between morphology and behavior in a population of free-living great tits (Parus major) monitored for seven years. In particular, we aimed to disentangle the effect of structural size versus body condition on risk-taking behavior. To do so, we repeatedly quantified multiple morphological (body mass, wing, tarsus, and bill length) and behavioral traits (aggressiveness and exploration) in 742 individual males. Structural equation modelling (SEM) allowed us to test causal a priori hypothesized relationships between the different morphological and behavioral traits. Our best-fitting SEM model supported the existence of a behavioral character, “risk-taking behavior” that covaried simultaneously with the latent variable “body size”, and “body condition”. Our findings thus demonstrate that an individual’s morphological and behavioral traits represent expressions of an integrated phenotype, suggesting a role for phenotypic integration in generating animal personality in a wild bird population

Data from: Does perceived predation risk affect patterns of extra-pair paternity? A field experiment in a passerine bird

1. Non-consumptive predator effects have been shown to influence a wide range of behavioural, life history, and morphological traits. Extra-pair reproduction is widespread among socially monogamous birds and may incur predation costs. Consequently, altered rates of extra-pair reproduction are expected in circumstances characterized by increased adult perceived predation risk. 2. Additionally, extra-pair reproduction is expected to be most affected for birds with phenotypes that generally increase predation risk (such as more active individuals). 3. In two consecutive years, perceived predation risk was manipulated for great tits, Parus major breeding in 12 nest-box plots by broadcasting sounds of their main predator (European sparrowhawk Accipiter nisus; 6 plots). As a control treatment, sounds of a sympatric, avian non-predator species were broadcasted (Eurasian blackbird, Turdus merula; 6 plots). 4. Levels of extra-pair paternity did not differ between plots with different predation-risk treatments. Males that moved more in a novel environment (more active or ‘faster exploring’) tended to have offspring with fewer partners, but this effect did not vary with predation-risk treatment. 5. From an adaptive viewpoint, predation costs associated with extra-pair reproduction may be small and may not outweigh the benefits of extra-pair behaviour. Research on a broader range of taxa with different mating strategies is now needed to confirm the generality of our findings