Among-individual Differences Research Articles

Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets.

Among-individual differences in behavior are now a widely studied research-focus within the field of behavioral ecology. Furthermore, elements of an animal's internal state, such as energy or fat reserves, and infection status can have large impacts on behaviors. Despite this, we still know little regarding how state may affect behavioral variation. Recent exposure to pathogens may have a particularly large impact on behavioral expression given that it likely activates costly immune pathways, potentially forcing organism to make behavioral tradeoffs. In this study we investigate how recent exposure to a common bacterial pathogen, Serratia marcescens, affects both the mean behavioral expression and the among-individual differences (i.e. variation) in boldness behavior in the field cricket, Gryllus integer. We find that recent pathogen exposure does not affect mean behavioral expression of the treatment groups, but instead affects behavioral variation and repeatability. Specifically, bacterial exposure drove large among-individual variation, resulting in high levels of repeatability in some aspects of boldness (willingness to emerge into a novel environment), but not others (latency to become active in novel environment), compared to non-infected crickets. Interestingly, sham injection resulted in a universal lack of among-individual differences. Our results highlight the sensitivity of among-individual variance and repeatability estimates to ecological and environmental factors that individuals face throughout their lives.

Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors

Animals typically display among-individual differences in behavior that are consistent over time (i.e., personality). These differences are often triggered by variable individual responses to environmental stress factors experienced during life, such as competition for resources and risk of predation. While the causes underlying animal personality are considered to be an issue of prime importance, it is still unknown whether personality emerges and develops over ontogeny if the main sources of behavioral differentiation are absent. Here, we tested whether personality emerged and was strengthened during the lifetime of Eastern mosquitofish (Gambusia holbrooki), once intraspecific competition and risk of predation were completely removed and genetic and maternal differences minimized. We found that individual differences in behavior were overall repeatable over ontogeny (i.e., personality was manifested). Personality was, however, not detectable in juvenile individuals but emerged during and after their sexual maturation. The emergence of personality was triggered by the decline in behavioral plasticity of individuals over ontogeny, while differences in behavior among individuals did not vary with age. Our results suggest that animal personality might be inevitable and emerge in fish under laboratory-controlled conditions even in absence of extrinsic factors that typically lead to behavioral differentiation. The decline of behavioral plasticity over lifetime might be a relevant mechanism for the development of personality in animals. Increasing evidence suggests that animals have personality, that is, individuals consistently differ in behavior among each other (e.g., bold and shy or social and non-social individuals). Personality differences among animals should be, by definition, consistent over time and often caused by environmental challenges experienced early in life. In this study, we observed that personality differences were not present at juvenile age in social fish but emerged later in their life, despite the fact that environmental challenges (i.e., predation risk and competition for space, food, and mates) were absent. Personality differences strengthened over lifetime, resulting from declines in individual behavioral plasticity. Our results suggest that the decline in behavioral plasticity with age may represent a relevant mechanism for behavioral differentiation in animals, in agreement with evidences from the human literature on age-related loss in behavioral plasticity.

Telomere length covaries with personality in wild brown trout

The prevalence of consistent among-individual differences in behaviour, or personality, makes adaptive sense if individuals differ in stable state variables that shift the balance between the costs and benefits of their behavioural decisions. These differences may give rise to both individual differences in, and covariance among, behaviours that influence an individual's exposure to risks. We here study the link between behaviour and a candidate state variable previously overlooked in the study of state-dependent personality variation: telomere length. Telomeres are the protective endcaps of chromosomes and their erosion with age is thought to play a crucial role in regulating organismal senescence and intrinsic lifespan. Following evidence that shorter telomeres may reduce the lifespan of animals in a wide range of taxa, we predict individuals with shorter telomeres to behave more boldly and aggressively. In order to test this, we measured telomere length and behaviour in wild juvenile brown trout (Salmo trutta). We found individuals with shorter fin telomeres to behave consistently more boldly and aggressively under controlled conditions in the laboratory. No such relationship was found with muscle telomere length 3–4months after the behavioural assays. We suggest that telomere dynamics are an important factor integrating personality traits with other state variables thought to be important in the regulation of behaviour, such as metabolism, disease resistance and growth.

Selection and constraints on offspring size-number trade-offs in sand lizards (Lacerta agilis).

The trade-off between offspring size and number is a central component of life-history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade-off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among-individual differences can mask individual trade-offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade-off between offspring size and number in a population of sand lizards by separating among- and within-individual patterns using a 15-year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade-off by investigating how a female's resource (condition)- vs. age-related size (snout-vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade-off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade-off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life-history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within-individual patterns can reveal trade-offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among-individual variation.

Responses to threat in a freshwater invader: longitudinal data reveal personality, habituation, and robustness to changing water temperatures in the "killer shrimp" Dikerogammarus villosus (Crustacea: Amphipoda).

Freshwater biodiversity and ecosystem integrity are under threat from biological invasions. The “killer shrimp” Dikerogammarus villosus is a highly predatory amphipod that has spread readily across Central Europe and recently the UK and its arrival has been associated with the significant loss of resident species. Despite this, studies of its behavioral ecology are sparse, even though its behavior may contribute to its invasion success. For the first time, we investigated antipredator “fleeing” behavior in D. villosus and how this changed with water temperature. Three key patterns emerged from our analysis. First, within a particular temperature condition there are moderate but consistent among-individual differences in behavior. These are driven by a combination of mean level among-individual differences and within-individual relative consistency in behavior, and provide the key marker for animal personalities. Second, the fleeing responses were not influenced by temperature and third, regardless of temperature, all individuals appeared to habituate to a repeated nondangerous stimulus, indicating a capacity for individual learning. We suggest that the antipredator behavior of D. villosus contributes to its rapid spread and that consistent among-individual differences in behavior may promote biological invasions across heterogeneous conditions. Robustness to changing water temperatures may also be potentially advantageous, particularly in an era of global climate change, where average temperatures could be elevated and less predictable.

Improved performance, within-individual consistency and between-individual differences in the righting behaviour of the Caribbean sea star, Oreaster reticulatus

Individuals cope differently to challenging and stressful situations. Being inverted is challenging and stressful for animals, as the position leaves them vulnerable to predators and desiccation. Although sea star self-righting was first studied in the 19th century, efforts to quantify patterns of within-individual consistency and among-individual differences are limited. Here we examined the performance and repeatability of righting behaviour in the Caribbean sea star (Oreaster reticulatus).Oreaster reticulatuswere wild caught and transported to a nearby facility where they were inverted up to five times. Most animals improved their righting times and exhibited within-individual consistency and among individual differences in righting method. We posit that it may be favourable to employ a consistent righting method to effectively achieve an upright position. Predation pressure and stress physiology are hypothesized to shape individual differences in righting behaviour. Moreover, these results provide preliminary evidence of personality in sea stars.

Exploration is dependent on reproductive state, not social state, in a cooperatively breeding bird.

Personality is an intriguing phenomenon in populations because it constrains behavioral flexibility. One theory suggests that personality could be generated and maintained if dependent on asset protection. It is predicted that trade-offs with fitness expectations and survival probability encourage consistent behavioral differences among individuals (personality). Although not mutually exclusive, the social niche specialization hypothesis suggests that a group of individuals that repeatedly interact will develop personality to avoid costly social conflict. The point at which behavioral consistency originates in the social niche hypothesis is still unclear, with predictions for development after a change in social status. In the facultative cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), residing on Cousin Island, breeding vacancies are limited and this forces individuals into different social roles. We used this system to test whether reproductive and social state predicted among-individual differences in exploration. We had 2 predictions. First, that an individual's start in life can predict personality, whereby young individuals with a good start to life (associated with early age reproduction and earlier onset survival senescence) are fast explorers, suggesting reproductive state-dependence. Second, that an individual's social status can predict personality, whereby dominant individuals will be fast explorers, suggesting that the behavior is social state-dependent. Neither of the behaviors was associated with social state and social state did not affect behavioral consistency. However, novel object exploration was associated with a proxy of reproductive state. Our results provide further support for state being a mechanism for generating individual differences in behavior.

Behaviour, metabolism and size: phenotypic modularity or integration in Acheta domesticus?

The pace-of-life hypothesis predicts that among-individual differences in behaviour should integrate with a wide variety of morphological, metabolic and life-history traits along a slow to fast pace-of-life continuum. Support for the pace-of-life hypothesis has been mixed, in part because most empirical tests have been conducted strictly at the phenotypic level and have thus conflated genetic and environmental sources of covariance among traits. In the present study, we tested the hypothesis that, according to the predictions of the pace-of-life hypothesis, body mass, routine metabolic rate, activity and exploratory propensity are positively integrated in the house cricket Acheta domesticus (Orthoptera: Gryllidae). Using modified open field behavioural tests and flow-through respirometry, we determined whether among-individual differences are correlated across morphology, behaviour and metabolism in 50 male house crickets. All traits were repeatable, but we found poor evidence for overall integration across traits. Instead we found evidence for modularity, with behavioural traits covarying independently from mass and routine metabolic rate. Modularity, like that found here between activity and exploratory propensity, has been suggested to facilitate adaptive evolutionary change by coupling functionally related traits into suites on which selection can act more rapidly.

Juvenile pathogen exposure affects the presence of personality in adult field crickets

Despite the ever increasing interest in animal personalities, i.e. among-individual variation in behavior, there are still several gaps in our understanding of how experiences during ontogeny influence the expression of behavior in adulthood. Immune challenges during ontogeny have been proposed to drive feedback loops between investment in immune function and personality type. In this study we investigate the effects of an early immune challenge, in the form of an introduced bacterial pathogen, on the development of personality in field crickets. Our results indicate that early pathogen exposure does not influence life history characteristics, immune response, or mean level of boldness behavior. Instead, early immune challenge affects the presence of personality later in the adult stage. Specifically, immune challenged individuals lack repeatability in some aspects of boldness behavior, indicating that among-individual variation is not present, while non-immune challenged individuals remain repeatable in their boldness behavior. This study joins a slowly growing body of literature indicating that experiences during ontogeny can have large influences on the among-individual differences in behaviors, thus affecting the presence of personality as adults.

Individual quality and personality: bolder males are less fecund in the hermit crab Pagurus bernhardus.

One explanation for animal personality is that different behavioural types derive from different life-history strategies. Highly productive individuals, with high growth rates and high fecundity, are assumed to live life at a fast pace showing high levels of boldness and risk taking, compared with less productive individuals. Here, we investigate among-individual differences in mean boldness (the inverse of the latency to recover from a startling stimulus) and in the consistency of boldness, in male hermit crabs in relation to two aspects of life-history investment. We assessed aerobic scope by measuring the concentration of the respiratory pigment haemocyanin, and we assessed fecundity by measuring spermatophore size. First, we found that individuals investing in large spermatophores also had high concentrations of haemocyanin. Using doubly hierarchical-generalized linear models to analyse longitudinal data on startle responses, we show that hermit crabs vary both in their mean response durations and in the consistency of their behaviour. Individual consistency was unrelated to haemocyanin concentration or spermatophore size, but mean startle response duration increased with spermatophore size. Thus, counter to expectations, it was the most risk-averse individuals, rather than the boldest and most risk prone, that were the most productive. We suggest that similar patterns should be present in other species, if the most productive individuals avoid risky behaviour.

Otolith-derived estimates of marine temperature use by West Greenland Atlantic salmon (Salmo salar)

Abstract Otolith-derived estimates of mean marine temperatures used by West Greenland 1SW Atlantic salmon (Salmo salar) of North American origin were determined for fish collected in 2009 and 2010. Otolith material corresponding to the second summer at sea was subsampled, via micro-milling, and analysed by mass spectrometry to produce stable oxygen isotope (δ18O) values from which temperature use estimates were obtained from a salmonid-based fractionation equation. Mean temperature estimates did not differ significantly by period (early vs. late summer), or capture year. The mean and variation estimates were also consistent with temperature use values previously published in the literature or derived from the limited number of data storage tags that have been retrieved for Atlantic salmon, with 80% of all individuals occupying temperatures in the 3.9–9.7°C range. Among-individual differences in temperature use did not correlate with measured otolith growth zone widths. Given the temporal, spatial and methodological variation associated with the derivation of marine temperature use estimates for Atlantic salmon, the data were interpreted to define a range of preferred temperatures within which among-individual differences in growth were driven by the interaction of feeding and temperature use, possibly as a result of the opportunistic feeding behaviour known to predominate among Atlantic salmon.

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.

How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model.

It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive–proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive-bred population of Xiphophorus birchmanni. We quantify among-individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11-ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy–bold) or coping style (reactive–proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11-ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among-individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive–reactive axis of integrated stress-coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.

The contribution of additive genetic variation to personality variation: heritability of personality.

Individual animals frequently exhibit repeatable differences from other members of their population, differences now commonly referred to as 'animal personality'. Personality differences can arise, for example, from differences in permanent environmental effects--including parental and epigenetic contributors--and the effect of additive genetic variation. Although several studies have evaluated the heritability of behaviour, less is known about general patterns of heritability and additive genetic variation in animal personality. As overall variation in behaviour includes both the among-individual differences that reflect different personalities and temporary environmental effects, it is possible for personality to be largely genetically influenced even when heritability of behaviour per se is quite low. The relative contribution of additive genetic variation to personality variation can be estimated whenever both repeatability and heritability are estimated for the same data. Using published estimates to address this issue, we found that approximately 52% of animal personality variation was attributable to additive genetic variation. Thus, while the heritability of behaviour is often moderate or low, the heritability of personality is much higher. Our results therefore (i) demonstrate that genetic differences are likely to be a major contributor to variation in animal personality and (ii) support the phenotypic gambit: that evolutionary inferences drawn from repeatability estimates may often be justified.

Dynamics of among-individual behavioral variation over adult lifespan in a wild insect.

Investigating patterns of among and within-individual trait variation in populations is essential to understanding how selection shapes phenotypes. Behavior is often the most flexible aspect of the phenotype, and to understand how it is affected by selection, we need to examine how consistent individuals are. However, it is not well understood whether among-individual differences tend to remain consistent over lifetimes, or whether the behavior of individuals relative to one another varies over time. We examined the dynamics of 4 behavioral traits (tendency to leave a refuge, shyness, activity, and exploration) in a wild population of field crickets (Gryllus campestris). We tagged individuals and then temporarily removed them from their natural environment and tested them under laboratory conditions. All 4 traits showed among-individual variance in mean levels of expression across the adult lifespan, but no significant differences in how rapidly expression changed with age. For all traits, among-individual variance increased as individuals got older. Our findings reveal seldom examined changes in variance components over the adult lifetime of wild individuals. Such changes will have important implications for the relationship between behavioral traits, life-histories, and fitness and the consequences of selection on wild individuals.

Interindividual variability in habitat use: evidence for a risk management syndrome in roe deer?

The way an individual reacts to the risk of predation or disturbance may have important consequences for its immediate and future survival. Risk is likely perceived differently by individuals in relation to among-individual differences in correlated behavioral traits, that is, syndromes or personalities. Given that animals can avoid the risk of predation/disturbance through modification of their habitat use, we might expect individuals of differing behavioral types to adopt contrasting tactics of habitat use when faced with risky or stressful situations. We studied the relationship between habitat use and among-individual variation in behavioral profile in a population of roe deer. We hypothesized that an individual's habitat use tactics should be related to their capacity to cope with risky situations. In particular, we predicted that more reactive (risk-averse) roe deer, with relatively high behavioral response and high body temperature at capture, long flight distances and which were more vigilant during feeding, should use riskier open habitat less, particularly when risk is high. We found that although the use of open habitat during the day was negatively correlated with the indices of reactivity at capture, it was also positively correlated with indices of reactivity while foraging in open habitat. Furthermore, most of the behavioral parameters we measured were intercorrelated and moderately repeatable, potentially indexing personality traits. We conclude that there is substantial interindividual variability in how individuals manage risky situations which imposes constraints on how they are able to exploit high-risk habitats, suggesting the existence of a risk management syndrome in this large herbivore.

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.

Tracking niche variation over millennial timescales in sympatric killer whale lineages

Niche variation owing to individual differences in ecology has been hypothesized to be an early stage of sympatric speciation. Yet to date, no study has tracked niche width over more than a few generations. In this study, we show the presence of isotopic niche variation over millennial timescales and investigate the evolutionary outcomes. Isotopic ratios were measured from tissue samples of sympatric killer whale Orcinus orca lineages from the North Sea, spanning over 10 000 years. Isotopic ratios spanned a range similar to the difference in isotopic values of two known prey items, herring Clupea harengus and harbour seal Phoca vitulina. Two proxies of the stage of speciation, lineage sorting of mitogenomes and genotypic clustering, were both weak to intermediate indicating that speciation has made little progress. Thus, our study confirms that even with the necessary ecological conditions, i.e. among-individual variation in ecology, it is difficult for sympatric speciation to progress in the face of gene flow. In contrast to some theoretical models, our empirical results suggest that sympatric speciation driven by among-individual differences in ecological niche is a slow process and may not reach completion. We argue that sympatric speciation is constrained in this system owing to the plastic nature of the behavioural traits under selection when hunting either mammals or fish.

LOCAL ADAPTATION WHEN COMPETITION DEPENDS ON PHENOTYPIC SIMILARITY

Recent work incorporating demographic-genetic interactions indicates the importance of population size, gene flow, and selection in influencing local adaptation. This work typically assumes that density-dependent survival affects individuals equally, but individuals in natural population rarely compete equally. Among-individual differences in resource use generate stronger competition between more similar phenotypes (frequency-dependent competition) but it remains unclear how this additional form of selection changes the interactions between population size, gene flow, and local stabilizing selection. Here, we integrate migration-selection dynamics with frequency-dependent competition. We developed a coupled demographic-quantitative genetic model consisting of two patches connected by dispersal and subject to local stabilizing selection and competition. Our model shows that frequency-dependent competition slightly increases local adaptation, greatly increases genetic variance within patches, and reduces the amount that migration depresses population size, despite the increased genetic variance load. The effects of frequency-dependence depend on the strength of divergent selection, trait heritability, and when mortality occurs in the life cycle in relation to migration and reproduction. Essentially, frequency-dependent competition reduces the density-dependent interactions between migrants and residents, the extent to which depends on how different and common immigrants are compared to residents. Our results add new dynamics that illustrate how competition can alter the effects of gene flow and divergent selection on local adaptation and population carrying capacities.

Breeding experience might be a major determinant of breeding probability in long-lived species: the case of the greater flamingo.

The probability of breeding is known to increase with age early in life in many long-lived species. This increase may be due to experience accumulated through past breeding attempts. Recent methodological advances allowing accounting for unobserved breeding episodes, we analyzed the encounter histories of 14716 greater flamingos over 25 years to get a detailed picture of the interactions of age and experience. Survival did not improve with experience, seemingly ruling out the selection hypothesis. Breeding probability varied within three levels of experience : no breeding experience, 1 experience, 2+ experiences. We fitted models with and without among-individual differences in breeding probabilities by including or not an additive individual random effect. Including the individual random effect improved the model fit less than including experience but the best model retained both. However, because modeling individual heterogeneity by means of an additive static individual random effect is currently criticized and may not be appropriate, we discuss the results with and without random effect. Without random effect, breeding probability of inexperienced birds was always times lower than that of same age experienced birds, and breeding probability increased more with one additional experience than with one additional year of age. With random effects, the advantage of experience was unequivocal only after age 9 while in young having experience was penalizing. Another pattern, that breeding probability of birds with experiences dropped after some age (8 without random effect; up to 11 with it), may point to differences in the timing of reproductive senescence or to the existence of a sensitive period for acquiring behavioral skills. Overall, the role of experience appears strong in this long-lived species. We argue that overlooking the role of experience may hamper detection of trade-offs and assessment of individual heterogeneity. However, manipulative experiments are desirable to confirm our finding.