Pace-of-life Syndrome Research Articles

Under pressure: human adolescents express a pace-of-life syndrome

The pace-of-life syndrome (POLS) hypothesis posits that life-history characteristics, among individual differences in behavior, and physiological traits have coevolved in response to environmental conditions. This hypothesis has generated much research interest because it provides testable predictions concerning the association between the slow-fast life-history continuum and behavioral and physiological traits. Although humans are among the most well-studied species and similar concepts exist in the human literature, the POLS hypothesis has not yet been directly applied to humans. Therefore, we aimed to (i) test predicted relationships between life history, physiology, and behavior in a human population and (ii) better integrate the POLS hypothesis with other similar concepts. Using data of a representative sample of German adolescents, we extracted maturation status for girls (menarche, n = 791) and boys (voice break, n = 486), and a set of health-related risk-taking behaviors and cardiovascular parameters. Maturation status and health-related risk behavior as well as maturation status and cardiovascular physiology covaried in boys and girls. Fast maturing boys and girls had higher blood pressure and expressed more risk-taking behavior than same-aged slow maturing boys and girls, supporting general predictions of the POLS hypothesis. Only some physiological and behavioral traits were positively correlated, suggesting that behavioral and physiological traits might mediate life-history trade-offs differently. Moreover, some aspects of POLS were sex-specific. Overall, the POLS hypothesis shares many similarities with other conceptual frameworks from the human literature and these concepts should be united more thoroughly to stimulate the study of POLS in humans and other animals. The pace-of-life syndrome (POLS) hypothesis suggests that life history, behavioral and physiological traits have coevolved in response to environmental conditions. Here, we tested this link in a representative sample of German adolescents, using data from a large health survey (the KIGGs study) containing information on individual age and state of maturity for girls and boys, and a set of health-related risk-taking behaviors and cardiovascular parameters. We found that fast maturing girls and boys had overall higher blood pressure and expressed more risk-taking behavior than same-aged slow maturing girls and boys. Only some behavioral and physiological traits were positively correlated, suggesting that behavioral and physiological traits might mediate life-history trade-offs differently and not necessarily form a syndrome. Our results demonstrate a general link between life history, physiological and behavioral traits in humans, while simultaneously highlighting a more complex and rich set of relationships, since not all relationships followed predictions by the POLS hypothesis.

Unravelling the relationships between life history, behaviour and condition under the pace-of-life syndromes hypothesis using long-term data from a wild bird

The hypothesis of pace-of-life syndromes (POLS) predicts relationships between traits including life history traits and risk-taking behaviour that can be mediated by the trade-off between current and future reproductive value. However, alternative causal mechanisms may also generate covariance among these traits without trade-offs. We investigated the relationships between survival to the next year, current reproductive investment and risk-taking behaviour (flight initiation distance) in male collared flycatchers, Ficedula albicollis, using long-term data. We used structural equation modelling (SEM) to uncover whether the associations among traits are mediated by a common latent factor that determines how individuals balance the trade-off between current and future reproductive value. As trade-offs could be concealed when there are differences in resource acquisition between individuals, we also included potential causes of these differences, body mass and body size, in the analysis. We found that risk-taking behaviour was positively related to reproductive investment and negatively to survival to the next year as could be predicted if investment into a risky behaviour is traded against future prospects. However, the most supported SEM model also suggested that survival to the next year was positively related to current reproductive investment, contrary to predictions of a hypothesis based on trade-off. These results remained qualitatively similar when controlling for body condition. In conclusion, we only could derive partial support for the POLS hypothesis. We suggest that aspects of individual quality, and not only trade-offs, should also be considered when interpreting the relationships between life history and behavioural traits. We investigated the association between two life history components (survival to the next year and current reproductive effort) and risk-taking behaviour, relying on long-term records from a passerine bird, to investigate the predictions of the pace-of-life syndrome (POLS) hypothesis. Using structural equation modelling, we found support for a causal model that implies that risk-taking negatively affects survival to the next year and that survival to the next year and current reproductive effort are strongly and positively associated. Controlling for the effect of body condition did not fundamentally change these relationships. We could not find conclusive evidence for the investigated traits being mediated by a common underlying factor, as generally predicted by the POLS hypothesis. However, the sign of the relationship between risk-taking behaviour and survival to the next year was as predicted by the POLS hypothesis.

Risk-taking behavior, urbanization and the pace of life in birds

Despite growing appreciation of the importance of considering a pace-of-life syndrome (POLS) perspective to understand how animals interact with their environment, studies relating behavior to life history under altered environmental conditions are still rare. By means of a comparative analysis of flight initiation distances (i.e., the distance at which an animal takes flight when a human being is approaching) across > 300 bird species distributed worldwide, we document here the existence of a POLS predicted by theory where slow-lived species tend to be more risk-averse than fast-lived species. This syndrome largely emerges from the influence of body mass, and is highly dependent on the environmental context. Accordingly, the POLS structure vanishes in urbanized environments due to slow-lived species adjusting their flight distances based on the perception of risk. While it is unclear whether changes in POLS reflect plastic and/or evolutionary adjustments, our findings highlight the need to integrate behavior into life history theory to fully understand how animals tolerate human-induced environmental changes. Animals can often respond to changing environmental conditions by adjusting their behavior. However, the degree to which different species can modify their behavior depends on their life history strategy and on the environmental context. Species-specific perception of risk is a conspicuous example of adjustable behavior tightly associated with life history strategy. While there is a general tendency of higher risk aversion in rural than city-dwelling birds, it is dependent on the species’ life history strategy. Slow-lived species are more prone to adjust their flight initiation distances based on the perception of risk, allowing humans to approach closer in urban than rural environments. Behavior must therefore be taken into account together with life history to reliably assess species’ vulnerability at the face of ongoing environmental change.

Models of pace-of-life syndromes (POLS): a systematic review

Variation in life history (LH) traits along the fast-slow continuum (referred to as pace of life, POL) is thought to result from a trade-off between investments in current versus future reproduction. Originally developed for understanding variation in LH strategies at the among-population level, the POL theory has more recently been applied towards understanding variation in LH traits at the within-population level, and further extended to address the covariance of LH traits with additional behavioural and/or physiological traits, referred to as pace-of-life syndromes (POLS). The article by Reale et al. (Philos T Roy Soc B 365:4051–4063, 2010), which synthesized several earlier reviews and opinions on among-individual covariation between LH, behavioural, and physiological traits, and subsequent research testing POLS in a variety of species, have collectively been cited several hundreds of times—a trend that continues. These works have interdisciplinary impact, informing research in life history biology, behavioural and developmental biology, and the social sciences. In this paper, we review the existing theoretical POLS models that provide adaptive explanations for covariances between LH traits and additional behavioural and/or physiological traits while assuming a trade-off between current and future reproduction. We find that the set of relevant models is small. Moreover, models show that covariances between life history traits and behavioural or physiological traits can arise even in the absence of a current-future reproduction trade-off, implying that observing such covariances does not provide a strong indication regarding the process generating POLS. We discuss lessons learned from existing models of POLS, highlight key gaps in the modelling literature, and provide guidelines for better integration between theory and data.

Behavioural mediators of genetic life-history trade-offs: a test of the pace-of-life syndrome hypothesis in field crickets.

The pace-of-life syndrome (POLS) hypothesis predicts associations between life history and 'risky' behaviours. Individuals with 'fast' lifestyles should develop faster, reproduce earlier, exhibit more risk-prone behaviours, and die sooner than those with 'slow' lifestyles. While support for POLS has been equivocal to date, studies have relied on individual-level (phenotypic) patterns in which genetic trade-offs may be masked by environmental effects on phenotypes. We estimated genetic correlations between life history (development, lifespan, size) and risky behaviours (exploration, aggression) in a pedigreed population of Mediterranean field crickets (Gryllus bimaculatus). Path analyses showed that behaviours mediated some genetic relationships between life history traits, though not those involved in trade-offs. Thus, while specific predictions of POLS theory were not supported, genetic integration of behaviour and life history was present. This implies a major role for risky behaviours in life history evolution.

Thermal physiology: A new dimension of the pace-of-life syndrome.

Current syndrome research focuses primarily on behaviour with few incorporating components of physiology. One such syndrome is the pace-of-life syndrome (POLS) which describes covariation between behaviour, metabolism, immunity, hormonal response, and life-history traits. Despite the strong effect temperature has on behaviour, thermal physiology has yet to be considered within this syndrome framework. We proposed the POLS to be extended to include a new dimension, the cold-hot axis. Under this premise, it is predicted that thermal physiology and behaviour would covary, whereby individual positioning along the thermal continuum would coincide with that of the behavioural continuum. This hypothesis was tested by measuring thermal traits of delicate skinks (Lampropholis delicata) and linking it to their behaviour. Principal components analysis and structural equation modelling were used to determine if traits were structured within the POLS and to characterize the direction of their interactions. Model results supported the inclusion of the cold-hot axis into the POLS and indicated that thermal physiology was the driver of this relationship, in that thermal traits either constrained or promoted activity, exploration, boldness and social behaviour. This study highlights the need to integrate thermal physiology within a syndrome framework.

Personality, immune response and reproductive success: an appraisal of the pace‐of‐life syndrome hypothesis

The pace-of-life syndrome (POLS) hypothesis is an extended concept of the life-history theory that includes behavioural traits. The studies challenging the POLS hypothesis often focus on the relationships between a single personality trait and a physiological and/or life-history trait. While pathogens represent a major selective pressure, few studies have been interested in testing relationships between behavioural syndrome, and several fitness components including immunity. The aim of this study was to address this question in the mealworm beetle, Tenebrio molitor, a model species in immunity studies. The personality score was estimated from a multidimensional syndrome based of four repeatable behavioural traits. In a first experiment, we investigated its relationship with two measures of fitness (reproduction and survival) and three components of the innate immunity (haemocyte concentration, and levels of activity of the phenoloxidase including the total proenzyme and the naturally activated one) to challenge the POLS hypothesis in T.molitor. Overall, we found a relationship between behavioural syndrome and reproductive success in this species, thus supporting the POLS hypothesis. We also showed a sex-specific relationship between behavioural syndrome and basal immune parameters. In a second experiment, we tested whether this observed relationship with innate immunity could be confirmed in term of differential survival after challenging by entomopathogenic bacteria, Bacillus thuringiensis. In this case, no significant relationship was evidenced. We recommend that future researchers on the POLS should control for differences in evolutionary trajectory between sexes and to pay attention to the choice of the proxy used, especially when looking at immune traits.

Inactive trout come out at night: behavioral variation, circadian activity, and fitness in the wild.

Theory suggests that high activity levels in animals increase growth at the cost of increased mortality. This growth-mortality tradeoff has recently been incorporated into the wider framework of the pace-of-life syndrome (POLS) hypothesis. However, activity is often quantified only in the laboratory and on a diurnal basis, leaving open the possibility that animals manage predation risk and feeding efficiency in the wild by modulating their circadian activity rhythms. Here we investigate how laboratory activity in wild brown trout parr (Salmo trutta L.) associates with circadian activity, growth, and mortality in their natal stream. We found that individuals with high activity in the laboratory displayed high dispersal and cathemeral activity in their natal stream. In contrast, trout with low laboratory activity showed variation of activity in the wild, which was negatively related to the light intensity. Our results do not support the growth-mortality trade-off of the POLS hypothesis as highly active, fast-growing individuals showed higher survival than inactive conspecifics. These novel results show for the first time that active and inactive individuals, as scored in the lab, can show different circadian patterns of behavior in the wild driven by light intensity. This implies that studies conducted under a narrow range of light conditions can bias our understanding of individual behavioral variation and its fitness consequences in the wild.

Unsociable juvenile male three-spined sticklebacks grow more attractive

An animal’s personality may be an adaptive behavioral response of individuals to consistent differences in physiology and life-history. Studying the relationship between behavior and other fitness-related traits within the pace-of-life syndrome (POLS) framework, which explains the integration of different traits using the concept of a fast-slow life-history continuum, may thus be a useful approach to understanding the evolution and maintenance of animal personality. According to the POLS hypothesis, for example, fast individuals should be behaviorally more active, bolder or less sociable, and potentially invest more in reproduction than slow individuals. Here, we examined whether the sociability of juvenile sticklebacks (Gasterosteus aculeatus) is linked with their key reproductive traits, carotenoid-based nuptial coloration of males and egg production of females. We also tested whether experimental manipulation of environmental conditions (control vs. warm winter) can change pace-of-life and the link between behavioral and reproductive traits. Male sticklebacks prone to shoaling expressed lower peak red coloration at the reproductive stage, during which they were solitary and territorial. In females, fecundity was not correlated with early social behavior. Experimental sticklebacks reared in warm winter conditions decreased their investment in reproduction, but the negative relationship between sociability and sexual signal of males was maintained. Our results suggest that the POLS could partly explain the maintenance of personality under predation pressure or severe mating competition. In natural environments, any benefit to sociable male sticklebacks may be counterbalanced by the cost of growing less attractive. Why do animals vary in personality, and how is such variation maintained within a population? An interesting approach for understanding this is studying how personality traits are correlated with other fitness-related traits within the pace-of-life framework. For the first time, our results show the link between sociability at the juvenile stage and the expression of sexual ornament during reproduction in male three-spined sticklebacks. Sociable juveniles may benefit from reduced predation risk, but they grow less attractive and this may reduce their mating success during reproduction. Thus, the trade-off between survival and reproduction may contribute to the maintenance of among-individual variation in behavior.

Do personalities co-vary with metabolic expenditure and glucocorticoid stress response in adult lizards?

Stable differences in physiology among individuals may facilitate the evolution of consistent individual differences in behavior. In particular, according to the pace-of-life syndrome (POLS) hypothesis, individual variation in metabolic expenditure and stress physiology should be linked with exploration, aggression, or risk taking behaviors. Previous studies have uncovered stable individual differences in metabolic expenditure and circulating glucorticoids in common lizards (Zootoca vivipara). We tested for correlations between standard metabolic rates (SMR), glucorticoid stress response and behavioral traits (activity, aggressiveness, risk taking and sociability) in males. In ectotherms, the thermal dependence of SMR should be included in the POLS hypothesis; we therefore measured SMR at three temperatures from rest to preferred body temperature. Activity, aggressiveness and risk taking, but not sociability, exhibited significant, short term repeatability, and little correlation was found between behavioral traits. The SMR of lizards with a low metabolism at rest increased faster with body temperature. The SMR at rest was negatively correlated with behavioral variation in sociability and activity but not with risk taking behavior. In addition, the plasma corticosterone level after an acute, handling stress increased slightly but not significantly with aggressiveness. We discuss alternative interpretations for these relationships and conclude that the link between inter-individual variation in physiology and behavior is trait-dependent in the common lizard.

Integrating the pace-of-life syndrome across species, sexes and individuals: covariation of life history and personality under pesticide exposure.

The pace-of-life syndrome (POLS) hypothesis integrates covariation of life-history traits along a fast-slow continuum and covariation of behavioural traits along a proactive-reactive personality continuum. Few studies have investigated these predicted life-history/personality associations among species and between sexes. Furthermore, whether and how contaminants interfere with POLS patterns remains unexplored. We tested for covariation patterns in life history and in behaviour, and for life-history/personality covariation among species, among individuals within species and between sexes. Moreover, we investigated whether pesticide exposure affects covariation between life history and behaviour and whether species and sexes with a faster POLS strategy have a higher sensitivity to pesticides. We reared larvae of four species of Ischnura damselflies in a common garden experiment with an insecticide treatment (chlorpyrifos absent/present) in the final instar. We measured four life-history traits (larval growth rate during the pesticide treatment, larval development time, adult mass and life span) and two behavioural traits (larval feeding activity and boldness, each before and after the pesticide treatment). At the individual level, life-history traits and behavioural traits aligned along a fast-slow and a proactive-reactive continuum, respectively. Species-specific differences in life history, with fast-lived species having a faster larval growth and development, a lower mass at emergence and a shorter life span, suggested that time constraints in the larval stage were predictably driving life-history evolution both in the larval stage and across metamorphosis in the adult stage. Across species, females were consistently more slow-lived than males, reflecting that a large body size and a long life span are generally more important for females. In contrast to the POLS hypothesis, there was only little evidence for the expected positive coupling between life-history pace and proactivity. Pesticide exposure decreased larval growth rate and affected life-history/personality covariation in the most fast-lived species. Our study supports the existence of life-history and behavioural continua with limited support for life-history/personality covariation. Variation in digestive physiology may explain this decoupling of life history and behaviour and provide valuable mechanistic insights to understand and predict the occurrence of life-history/personality covariation patterns.

Metabolism, personality and pace of life in the Trinidadian guppy, Poecilia reticulata

While among-individual variation in behaviour, or personality, is common across taxa, its mechanistic underpinnings are poorly understood. The Pace of Life syndrome (POLS) provides one possible explanation for maintenance of personality differences. POLS predicts that metabolic differences will covary with behavioural variation, with high metabolism associated with risk prone behaviour and ‘faster’ life histories (e.g., high growth, early maturation). We used a repeated measures approach, assaying metabolic traits (rate and scope), behaviour and growth to test these predictions in the Trinidadian guppy,Poecilia reticulata. We found that while individuals varied significantly in their behaviour and growth rate, more risk prone individuals did not grow significantly faster. Furthermore, after accounting for body size there was no support for among-individual variation in metabolic traits. Thus, while personality differences are clearly present in this population, they do not covary with metabolism and the POLS framework is not supported.

Exploration behavior and parental effort in wild great tits: partners matter

The extended pace-of-life syndrome (POLS) hypothesis suggests that variation in boldness-like behaviors has co-evolved with variation in life-history strategies within populations, yet both theoretically driven experiments and evidence for phenotypic correlations between boldness-like behaviors and reproduction-related activities are scarce. Here we test the prediction that more exploratory individuals should be willing to provide more effort into current reproduction than less exploratory ones by investigating the association between exploration behavior and parental effort in wild great tits (Parus major). To this end, we assessed exploration behavior following a standardized assay. Then, we estimated individual willingness to provide parental effort into brood provisioning as (1) individual increase in nest visit rate after the brood had been artificially enlarged and (2) individual latency to return to the nest after this manipulation. Fast male explorers were quicker than slow explorers to return to the nest after the manipulation. Males paired with a partner of similar exploration score—either a fast or slow female explorer —increased their nest visit rate more than males paired with a partner of dissimilar exploration score. The relationship between exploration and parental effort then depended on one’s partner’s behavior. Our test thus provides only partial support for the extended POLS hypothesis and highlights the potential importance of the social environment in shaping the relationship between boldness-like behaviors and fitness-maximizing traits.

Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young?

The pace-of-life syndrome (POLS) hypothesis for animal personality proposes that variation among individuals in life-history strategies is associated with consistent differences in behavior. We tested predictions of this hypothesis in the superb fairy-wren, Malurus cyaneus, by investigating long-term individual differences in risk-related behaviors (latency to enter a novel artificial environment, exploration, activity and response to mirror image stimulation) and survival. We found consistent differences between individuals in these behaviors (adjusted repeatability of exploration of artificial novel environment = 0.37). Individual differences were consistent over several years and bi-variate analyses showed a significant among-individual correlation (‘behavioral syndrome’) between exploration behavior at two life stages (young adult and old adult). Docility at the nestling stage predicted exploration behavior of juveniles. Behavioral traits measured in a risky context were correlated with one another, forming a behavioral syndrome of coping strategies ranging from ‘proactive’ to ‘reactive’. Nestlings that were more active and exploratory in isolation were less docile during handling, while adults that entered the artificial environment fast were more exploratory, active, and aggressive in the artificial environment. Exploration behavior increased within individuals as they aged and when they were in poorer condition, consistent with expectations of more risk-prone behavior with lower residual reproductive value (reduced ‘asset protection’). Risk-related behavior predicted the probability of apparent survival: more exploratory individuals were less likely to be present in the population twelve months later. Our findings suggest that, consistent with the predictions of the POLS hypothesis, individual variation in survival is associated with consistent individual differences in risk-related behavior that are maintained long-term and span developmental boundaries.

Behavioural consistency and life history of Rana dalmatina tadpoles.

The focus of evolutionary behavioural ecologists has recently turned towards understanding the causes and consequences of behavioural consistency, manifesting either as animal personality (consistency in a single behaviour) or behavioural syndrome (consistency across more behaviours). Behavioural type (mean individual behaviour) has been linked to life-history strategies, leading to the emergence of the integrated pace-of-life syndrome (POLS) theory. Using Rana dalmatina tadpoles as models, we tested if behavioural consistency and POLS could be detected during the early ontogenesis of this amphibian. We targeted two ontogenetic stages and measured activity, exploration and risk-taking in a common garden experiment, assessing both individual behavioural type and intra-individual behavioural variation. We observed that activity was consistent in all tadpoles, exploration only became consistent with advancing age and risk-taking only became consistent in tadpoles that had been tested, and thus disturbed, earlier. Only previously tested tadpoles showed trends indicative of behavioural syndromes. We found an activity-age at metamorphosis POLS in the previously untested tadpoles irrespective of age. Relative growth rate correlated positively with the intra-individual variation of activity of the previously untested older tadpoles. In previously tested older tadpoles, intra-individual variation of exploration correlated negatively and intra-individual variation of risk-taking correlated positively with relative growth rate. We provide evidence for behavioural consistency and POLS in predator- and conspecific-naive tadpoles. Intra-individual behavioural variation was also correlated to life history, suggesting its relevance for the POLS theory. The strong effect of moderate disturbance related to standard behavioural testing on later behaviour draws attention to the pitfalls embedded in repeated testing.

Elevational trends in life histories: revising the pace‐of‐life framework

Life-history traits in birds, such as lifespan, age at maturity, and rate of reproduction, vary across environments and in combinations imposed by trade-offs and limitations of physiological mechanisms. A plethora of studies have described the diversity of traits and hypothesized selection pressures shaping components of the survival-reproduction trade-off. Life-history variation appears to fall along a slow-fast continuum, with slow pace characterized by higher investment in survival over reproduction and fast pace characterized by higher investment in reproduction over survival. The Pace-of-Life Syndrome (POLS) is a framework to describe the slow-fast axis of variation in life-history traits and physiological traits. The POLS corresponds to latitudinal gradients, with tropical birds exhibiting a slow pace of life. We examined four possible ways that the traits of high-elevation birds might correspond to the POLS continuum: (i) rapid pace, (ii) tropical slow pace, (iii) novel elevational pace, or (iv) constrained pace. Recent studies reveal that birds breeding at high elevations in temperate zones exhibit a combination of traits creating a unique elevational pace of life with a central trade-off similar to a slow pace but physiological trade-offs more similar to a fast pace. A paucity of studies prevents consideration of the possibility of a constrained pace of life. We propose extending the POLS framework to include trait variation of elevational clines to help to investigate complexity in global geographic patterns.

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.