Manipulating monoamines reduces exploration and boldness of Mediterranean field crickets.

Despite the prevalence and research interest of animal personality, its underlying mechanisms are not yet fully understood. Due to the essential role of monoamines in modulating behaviour, we manipulated the monoaminergic systems of Mediterranean field crickets (Gryllus bimaculatus) to explore whether this altered behavioural responses commonly used to describe animal personality. Previous work has shown that both serotonin and dopamine manipulations can alter cricket behaviour, although results differ depending on the drug in focus. Here, we investigate the effect of Fluphenazine, a dopamine antagonist which also interacts with serotonin receptors, on activity, exploration, boldness, and aggression. These results are compared with those of our earlier work that investigated the effect of drugs that more specifically target serotonin or dopamine systems (Fluoxetine and Ropinirole, respectively). Due to limited research on dose-effects of Fluphenazine, we created dose-response curves with concentrations ranging from those measured in surface waters up to human therapeutic doses. We show that compared to control animals, Fluphenazine manipulation resulted in lower levels of both exploration and boldness, but did not affect activity nor aggression. The effect on explorative behaviour contradicts our previous results of serotonin and dopamine manipulations. These results together confirm the causal role of monoamines in explaining variation in behaviour often used to describe animal personality, effects that can be both dose- and behaviour-dependent. Further, our results suggest that previous results assigned specifically to the dopaminergic system, may at least partly be explained by effects of the serotonergic system. Thus, future studies should continue to investigate the explicit underlying roles of specific monoamines in explaining behavioural variation.

The relationship between monoaminergic gene expression, learning, and optimism in red junglefowl chicks.

Intra-species cognitive variation is commonly observed, but explanations for why individuals within a species differ in cognition are still understudied and not yet clear. Cognitive processes are likely influenced by genetic differences, with genes in the monoaminergic systems predicted to be important. To explore the potential role of these genes in association with individual variation in cognition, we exposed red junglefowl (Gallus gallus) chicks to behavioural assays measuring variation in learning (discriminative learning, reversal learning, and cognitive flexibility) and optimism (measured in a cognitive judgement bias test). Following this, we analysed prefrontal cortex gene expression of several dopaminergic and serotonergic genes in these chicks. Of our explored genes, serotonin receptor genes 5HT2A and 5HT2B, and dopaminergic receptor gene DRD1 were associated with measured behaviour. Chicks that had higher 5HT2A were less flexible in the reversal learning task, and chicks with higher 5HT2B also tended to be less cognitively flexible. Additionally, chicks with higher DRD1 were more optimistic, whilst chicks with higher 5HT2A tended to be less optimistic. These results suggest that the serotonergic and dopaminergic systems are linked to observed cognitive variation, and, thus, individual differences in cognition can be partially explained by variation in brain gene expression.

Individual variation in age-dependent reproduction: Fast explorers live fast but senesce young?

Adaptive integration of life history and behaviour is expected to result in variation in the pace-of-life. Previous work focused on whether 'risky' phenotypes live fast but die young, but reported conflicting support. We posit that individuals exhibiting risky phenotypes may alternatively invest heavily in early-life reproduction but consequently suffer greater reproductive senescence. We used a 7-year longitudinal dataset with >1,200 breeding records of >800 female great tits assayed annually for exploratory behaviour to test whether within-individual age dependency of reproduction varied with exploratory behaviour. We controlled for biasing effects of selective (dis)appearance and within-individual behavioural plasticity. Slower and faster explorers produced moderate-sized clutches when young; faster explorers subsequently showed an increase in clutch size that diminished with age (with moderate support for declines when old), whereas slower explorers produced moderate-sized clutches throughout their lives. There was some evidence that the same pattern characterized annual fledgling success, if so, unpredictable environmental effects diluted personality-related differences in this downstream reproductive trait. Support for age-related selective appearance was apparent, but only when failing to appreciate within-individual plasticity in reproduction and behaviour. Our study identifies within-individual age-dependent reproduction, and reproductive senescence, as key components of life-history strategies that vary between individuals differing in risky behaviour. Future research should thus incorporate age-dependent reproduction in pace-of-life studies.

Author Correction: Adaptive individual variation in phenological responses to perceived predation levels.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Effects of monoamine manipulations on the personality and gene expression of three-spined sticklebacks.

Among-individual behavioral differences (i.e. animal personality) are commonly observed across taxa, although the underlying, causal mechanisms of such differences are poorly understood. Animal personality has been correlated with physiological functions as well as fitness-related traits. Variation in many aspects of monoamine systems, such as metabolite levels and gene polymorphisms, has been linked to behavioral variation. Therefore, here we experimentally investigated the potential role of monoamines in explaining individual variation in personality, using two common pharmaceuticals that respectively alter the levels of serotonin and dopamine in the brain: fluoxetine and ropinirole. We exposed three-spined sticklebacks, a species that shows animal personality, to either chemical alone or to a combination of the two chemicals, for 18 days. During the experiment, fish were assayed at four time points for the following personality traits: exploration, boldness, aggression and sociability. To quantify brain gene expression on short- and longer-term scales, fish were sampled at two time points. Our results show that monoamine manipulations influence fish behavior. Specifically, fish exposed to either fluoxetine or ropinirole were significantly bolder, and fish exposed to the two chemicals together tended to be bolder than control fish. Our monoamine manipulations did not alter the gene expression of monoamine or stress-associated neurotransmitter genes, but control, untreated fish showed covariation between gene expression and behavior. Specifically, exploration and boldness were predicted by genes in the dopaminergic, serotonergic and stress pathways, and sociability was predicted by genes in the dopaminergic and stress pathways. These results add further support to the links between monoaminergic systems and personality, and show that exposure to monoamines can causally alter animal personality.

Adaptive individual variation in phenological responses to perceived predation levels.

The adaptive evolution of timing of breeding (a component of phenology) in response to environmental change requires individual variation in phenotypic plasticity for selection to act upon. A major question is what processes generate this variation. Here we apply multi-year manipulations of perceived predation levels (PPL) in an avian predator-prey system, identifying phenotypic plasticity in phenology as a key component of alternative behavioral strategies with equal fitness payoffs. We show that under low-PPL, faster (versus slower) exploring birds breed late (versus early); the pattern is reversed under high-PPL, with breeding synchrony decreasing in conjunction. Timing of breeding affects reproductive success, yet behavioral types have equal fitness. The existence of alternative behavioral strategies thus explains variation in phenology and plasticity in reproductive behavior, which has implications for evolution in response to anthropogenic change.

Experimental manipulation of monoamine levels alters personality in crickets.

Animal personality has been described in a range of species with ecological and evolutionary consequences. Factors shaping and maintaining variation in personality are not fully understood, but monoaminergic systems are consistently linked to personality variation. We experimentally explored how personality was influenced by alterations in two key monoamine systems: dopamine and serotonin. This was done using ropinirole and fluoxetine, two common human pharmaceuticals. Using the Mediterranean field cricket (Gryllus bimaculatus), we focused on the personality traits activity, exploration, and aggression, with confirmed repeatability in our study. Dopamine manipulations explained little variation in the personality traits investigated, while serotonin manipulation reduced both activity and aggression. Due to limited previous research, we created a dose-response curve for ropinirole, ranging from concentrations measured in surface waters to human therapeutic doses. No ropinirole dose level strongly influenced cricket personality, suggesting our results did not come from a dose mismatch. Our results indicate that the serotonergic system explains more variation in personality than manipulations of the dopaminergic system. Additionally, they suggest that monoamine systems differ across taxa, and confirm the importance of the mode of action of pharmaceuticals in determining their effects on behaviour.

Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social.

ABSTRACT: The existence of animal personality is now well-documented, although the causes and consequences of this phenomenon are still largely unclear. Parasite infection can have pervasive effects on hosts, including altering host behaviour, and may thus contribute to differences in host personality. We investigated the relationship between the three-spined stickleback and its common parasite Glugea anomala, with focus on differences in host personality. Naturally infected and uninfected individuals were assayed for the five personality traits activity, exploration, boldness, sociability, and aggression. If infected fish behaved differently from uninfected, to benefit this parasite with horizontal transmission, we predicted behaviour increasing interactions with other sticklebacks to increase. Infection status explained differences in host personality. Specifically, Glugea-infected individuals were more social than uninfected fish. This confirms a link between parasite infection and host behaviour, and a relationship which may improve the horizontal transmission of Glugea. However, future studies need to establish the consequences of this for the parasite, and the causality of the parasite-host personality relationship. SIGNIFICANCE STATEMENT: Parasite infection that alters host behaviour could be a possible avenue of research into the causes of animal personality. We studied the link between infection and personality using the three-spined stickleback and its parasite Glugea anomala. We predicted that infected individuals would be more prone to interact with other sticklebacks, since this would improve transmission of this parasite. The personality of uninfected and naturally infected fish was measured and we observed that Glugea-infected sticklebacks were more social. Our results confirm a link between parasitism and variation in host personality.

The Influence of Rearing on Behavior, Brain Monoamines, and Gene Expression in Three-Spined Sticklebacks.

The causes of individual variation in behavior are often not well understood, and potential underlying mechanisms include both intrinsic and extrinsic factors, such as early environmental, physiological, and genetic differences. In an exploratory laboratory study, we raised three-spined sticklebacks (Gasterosteus aculeatus) under 4 different environmental conditions (simulated predator environment, complex environment, variable social environment, and control). We investigated how these manipulations related to behavior, brain physiology, and gene expression later in life, with focus on brain dopamine and serotonin levels, turnover rates, and gene expression. The different rearing environments influenced behavior and gene expression, but did not alter monoamine levels or metabolites. Specifically, compared to control fish, fish exposed to a simulated predator environment tended to be less aggressive, more exploratory, and more neophobic; and fish raised in both complex and variable social environments tended to be less neophobic. Exposure to a simulated predator environment tended to lower expression of dopamine receptor DRD4A, a complex environment increased expression of dopamine receptor DRD1B, while a variable social environment tended to increase serotonin receptor 5-HTR2B and serotonin transporter SLC6A4A expression. Despite both behavior and gene expression varying with early environment, there was no evidence that gene expression mediated the relationship between early environment and behavior. Our results confirm that environmental conditions early in life can affect phenotypic variation. However, the mechanistic pathway of the monoaminergic systems translating early environmental variation into observed behavioral responses was not detected.

Do great tits (Parus major) suppress basal metabolic rate in response to increased perceived predation danger? A field experiment.

Several studies have shown that individuals with higher metabolic rates (MRs) feed at higher rates and are more willing to forage in the presence of predators. This increases the acquisition of resources, which in turn, may help to sustain a higher MR. Elevated predation danger may be expected to result in reduced MRs, either as a means of allowing for reduced feeding and risk-taking, or as a consequence of adaptively reducing intake rates via reduced feeding and/or risk-taking. We tested this prediction in free-living great tits (Parus major) using a playback experiment to manipulate perceived predation danger. There was evidence that changes in body mass and BMR differed as a function of treatment. In predator treatment plots, great tits tended to reduce their body mass, a commonly observed response in birds to increased predation danger. In contrast, birds from control treatment plots showed no overall changes in body mass. There was also evidence that great tits from control treatment plots increased their basal metabolic rate (BMR) over the course of the experiment, presumably due to decreasing ambient temperatures over the study period. However, there was no evidence for changes in BMR for birds from predator treatment plots. Although the directions of these results are consistent with the predicted directions of effects, the effects sizes and confidence intervals yield inconclusive support for the hypothesis that great tits would adaptively suppress BMR in response to increased perceived predation risk. The effect size observed in the present study was small (~1%) and would not be expected to result in substantive reductions in feeding rate and/or risk-taking. Whether or not ecological conditions that generate greater energetic stress (e.g. lower food availability, lower ambient temperatures) could produce an effect that produces biologically meaningful reductions in feeding activity and/or risk-taking remains an open question.