Population-, sex- and individual level divergence in life-history and activity patterns in an annual killifish.

Variation in life-history strategies along a slow-fast continuum is largely governed by life-history trade-offs. The pace-of-life syndrome hypothesis (POLS) expands on this idea and suggests coevolution of these traits with personality and physiology at different levels of biological organization. However, it remains unclear to what extent covariation at different levels aligns and if also behavioral patterns such as diurnal activity changes should be incorporated. Here, we investigate variation in life-history traits as well as behavioral variation at the individual, sex and population level in the Turquoise killifish Nothobranchius furzeri. We performed a common garden laboratory experiment with four populations that differ in pond permanence and scored life-history and behavioral (co-) variation at the individual and population level for both males and females. In addition, we focused on diurnal activity change as a behavioral trait that remains understudied in ecology. Our results demonstrate sex-specific variation in adult body size and diurnal activity change among populations that originate from ponds with differences in permanence. However, there was no pond permanence-dependent divergence in maturation time, juvenile growth rate, fecundity and average activity level. With regard to behavior, individuals differed consistently in locomotor activity and diurnal activity change while, in contrast with POLS predictions, we found no indications for life-history and behavioral covariation at any level. Overall, this study illustrates that diurnal activity change differs consistently between individuals, sexes and populations although this variation does not appear to match POLS predictions.

Bold perch live life in the fast lane.

A schematic summary showing the links between behaviour and life-history observed by Nakayama, Rapp & Arlinghaus in wild Eurasion perch (Perca fluviatilis). [Colour figure can be viewed at wileyonlinelibrary.com]. In Focus: Nakayama, S., Rapp, T. & Arlinghaus, R. (2017) Fast-slow life history is correlated with individual differences in movements and prey selection in an aquatic predator in the wild. Journal of Animal Ecology, 86, 192-201. The pace-of-life syndrome hypothesis (POLS) suggests that individual behavioural variation co-evolves with life-history variation, causing individuals on a fast life-history trajectory to display more active or bold personalities than individuals following a slow trajectory. In the present study, Nakayama, Rapp & Arlinghaus () followed the detailed movement patterns of wild Eurasian perch using acoustic telemetry and studied their relationships with life-history traits inferred from scale samples. Consistent with POLS, individuals with greater reproductive effort changed more often between active and passive behavioural modes. Moreover, individuals growing fast as a juvenile stayed active longer and moved over greater distances when adult. This study shows compelling evidence for covariance between personality and pace-of-life in a natural population.

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.

Generalist-specialist trade-off during thermal acclimation.

The shape of performance curves and their plasticity define how individuals and populations respond to environmental variability. In theory, maximum performance decreases with an increase in performance breadth. However, reversible acclimation may counteract this generalist-specialist trade-off, because performance optima track environmental conditions so that there is no benefit of generalist phenotypes. We tested this hypothesis by acclimating individual mosquitofish (Gambusia holbrooki) to cool and warm temperatures consecutively and measuring performance curves of swimming performance after each acclimation treatment. Individuals from the same population differed significantly in performance maxima, performance breadth and the capacity for acclimation. As predicted, acclimation resulted in a shift of the temperature at which maximal performance occurred. Within acclimation treatments, there was a significant generalist-specialist trade-off in responses to acute temperature change. Surprisingly, however, there was also a trade-off across acclimation treatments, and animals with greater capacity for cold acclimation had lower performance maxima under warm conditions. Hence, cold acclimation may be viewed as a generalist strategy that extends performance breadth at the colder seasons, but comes at the cost of reduced performance at the warmer time of year. Acclimation therefore does not counteract a generalist-specialist trade-off and, at least in mosquitofish, the trade-off seems to be a system property that persists despite phenotypic plasticity.

Individual and sex-specific differences in intrinsic growth rate covary with consistent individual differences in behaviour.

The evolutionary causes of consistent individual differences in behaviour are currently a source of debate. A recent hypothesis suggests that consistent individual differences in life-history productivity (growth and/or fecundity) may covary with behavioural traits that contribute to growth-mortality trade-offs, such as risk-proneness (boldness) and foraging activity (voraciousness). It remains unclear, however, to what extent individual behavioural and life-history profiles are set early in life, or are a more flexible result of specific environmental or developmental contexts that allow bold and active individuals to acquire more resources. Longitudinal studies of individually housed animals under controlled conditions can shed light on this question. Since growth and behaviour can both vary within individuals (they are labile), studying between-individual correlations in behaviour and growth rate requires repeated scoring for both variables over an extended period of time. However, such a study has not yet been done. Here, we repeatedly measured individual mass seven times each, boldness 40 times each and voracity eight times each during the first 4 months of life on 90 individually housed crayfish (Cherax destructor). Animals were fed ad libitum, generating a context where individuals can express their intrinsic growth rate (i.e. growth capacity), but in which bold and voracious behaviour is not necessary for high resource acquisition (crayfish can and do hoard food back to their burrow). We show that individuals that were consistently bold over time during the day were also bolder at night, were more voracious and maintained higher growth rates over time than shy individuals. Independent of individual differences, we also observed that males were faster-growing, bolder and more voracious than females. Our findings imply that associations between bold behaviour and fast growth can occur in unlimited food contexts where there is no necessary link between bold behaviour and resource acquisition - offering support for the 'personality-productivity' hypothesis. We suggest future research should study links between consistent individual differences in behaviour and life history under a wider range of contexts, in order to shed light on the role of biotic and abiotic conditions in the strength, direction and stability of their covariance.

Predictability as a personality trait: consistent differences in intraindividual behavioral variation.

Although animal behavior is generally repeatable, most behavioral variation apparently occurs within rather than across individuals. With the exception of very recent interest in individual behavioral plasticity (consistent differences in responsiveness), this within-individual variation has been largely ignored despite its importance in the study of proximate and ultimate questions about behavior. Here, we repeatedly scored the undisturbed activity of 30 adult male mosquitofish across multiple observation bouts spanning 132 days ([Formula: see text] observations per fish). We found that the behavior of some individuals was consistently more predictable in a given context than others. Repeatability for this "intraindividual variation" (IIV; [Formula: see text]) was evident after accounting for individual differences in activity trends across days, and activity responses due to fine-scale temperature variation (i.e., individual plasticity in response to both variables). To our knowledge, this is the first evidence that predictability of behavior is a repeatable characteristic of individual animals. We suggest that IIV represents an important axis of consistent behavioral variation that has previously not been formally considered. Finally, individual differences in predictability may similarly exist for labile morphological and physiological traits but have seemingly not been studied.

Natural selection, plasticity and the emergence of a behavioural syndrome in the wild.

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2-month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open-field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.