A Behavioral Syndrome Linking Boldness and Flexibility Facilitates Invasion Success in Sticklebacks.

AbstractFor a species to expand its range, it needs to be good at dispersing and also capable of exploiting resources and adapting to different environments. Therefore, behavioral and cognitive traits could play key roles in facilitating invasion success. Marine threespined sticklebacks (Gasterosteus aculeatus) have repeatedly colonized freshwater environments and rapidly adapted to them. Here, by comparing the behavior of hundreds of lab-reared sticklebacks from six different populations, we show that marine sticklebacks are bold, while sticklebacks that have become established in freshwater lakes are flexible. Moreover, boldness and flexibility are negatively correlated with one another at the individual, family, and population levels. These results support the hypothesis that boldness is favored in invaders during the initial dispersal stage, while flexibility is favored in recent immigrants during the establishment stage, and they suggest that the link between boldness and flexibility facilitates success during both the dispersal stage and the establishment stage. This study adds to the growing body of work showing the importance of behavioral correlations in facilitating colonization success in sticklebacks and other organisms.

Predictors of individual variation in reversal learning performance in three-spined sticklebacks.

Behavioral flexibility is a type of phenotypic plasticity that can influence how animals cope with environmental change and is often measured with a reversal learning paradigm. The goal of this study was to understand why individuals differ in behavioral flexibility, and whether individual differences in behavioral flexibility fit the predictions of coping styles theory. We tested whether individual variation in flexibility correlates with response to novelty (response to a novel object), boldness (emergence into a novel environment), and behavioral persistence (response to a barrier), and tested for trade-offs between how quickly individuals learn an initial discrimination and flexibility. We compare results when reversal learning performance is measured during an early step of reversal learning (e.g. the number of errors during the first reversal session) to when reversal learning performance is measured by time to criterion. Individuals that made fewer mistakes during an early step of reversal learning spent more time away from the novel object, were less bold, less persistent, and performed worse during initial discrimination learning. In contrast, time to criterion was not correlated with any of the behaviors measured. This result highlights the utility of dissecting the steps of reversal learning to better understand variation in behavioral flexibility. Altogether, this study suggests that individuals differ in flexibility because flexibility is a key ingredient to their overall integrated strategy for coping with environmental challenges.

Neurogenomic insights into paternal care and its relation to territorial aggression.

Motherhood is characterized by dramatic changes in brain and behavior, but less is known about fatherhood. Here we report that male sticklebacks-a small fish in which fathers provide care-experience dramatic changes in neurogenomic state as they become fathers. Some genes are unique to different stages of paternal care, some genes are shared across stages, and some genes are added to the previously acquired neurogenomic state. Comparative genomic analysis suggests that some of these neurogenomic dynamics resemble changes associated with pregnancy and reproduction in mammalian mothers. Moreover, gene regulatory analysis identifies transcription factors that are regulated in opposite directions in response to a territorial challenge versus during paternal care. Altogether these results show that some of the molecular mechanisms of parental care might be deeply conserved and might not be sex-specific, and suggest that tradeoffs between opposing social behaviors are managed at the gene regulatory level.

Social environment determines the effect of boldness and activity on survival.

Populations of animals are composed of individuals that differ in ecologically relevant behaviors. Building evidence also suggests that individuals occupy different social niches. Here, in a mark-recapture experiment, we show evidence of an interacting effect of behavior and social niche on survival in the wild: bold individuals had higher survival if they were initially captured in groups while shy, inactive individuals had higher survival if they were initially captured when alone. These findings provide support for the hypothesis that behavioral type-environment correlations can be favored by natural selection.

Intraspecific variation in cue-specific learning in sticklebacks.

Animals must identify reliable cues amidst environmental noise during learning, and the cues that are most reliable often depend on the local ecology. Comparing the performance of populations of the same species across multiple versions of a cognitive task can reveal whether some populations learn to use certain cues faster than others. Here, using a criterion-based protocol, we assessed whether two natural populations of sticklebacks differed in how quickly they learned to associate two different discrimination cues with the location of food. One version of the discrimination task required animals to use visual (colour) cues while the other required animals to use egocentric (side) cues. There were significant behavioural differences between the two populations, but no evidence that one population was generally better at learning, or that one version of the task was generally harder than the other. However, the two populations excelled on different tasks: fish from one population performed significantly better on the side version than they did on the colour version, while the opposite was observed in the other population. These results suggest that the two populations are equally capable of discrimination learning, but are primed to form associations with different cues. Ecological differences between the populations in environmental stability might account for the observed variation in learning. These findings highlight the value of comparing cognitive performance on different variations of the same task in order to understand variation in cognitive mechanisms.

Testing the predictions of coping styles theory in threespined sticklebacks.

Coping styles theory provides a framework for understanding individual variation in how animals respond to environmental change, and predicts how individual differences in stress responsiveness and behavior might relate to cognitive differences. According to coping styles theory, proactive individuals are bolder, less reactive to stressors, and more routinized than their reactive counterparts. A key tenet of coping styles theory is that variation in coping styles is maintained by tradeoffs with behavioral flexibility: proactive individuals excel in stable environments while more flexible, reactive individuals perform better in variable environments. Here, we assess evidence for coping styles within a natural population of threespined sticklebacks (Gasterosteus aculeatus). We developed a criterion-based learning paradigm to evaluate individual variation in initial and reversal learning. We observed strong individual differences in boldness, cortisol production, and learning performance. Consistent with coping styles, fish that released more cortisol were more timid in response to a predator attack and slower to learn a color discrimination task. However, there was no evidence that reactive individuals performed better when the environment changed (when the rewarded color was reversed). The failure to detect trade-offs between behavioral routinization and flexibility prompts other explanations for the maintenance of differing coping styles.