Learning is ubiquitous in the animal kingdom but has been studied extensively in only a handful of species. Moreover, learning studied under laboratory conditions is typically unrelated to the animal's natural environment or life history. Here, we designed a task relevant to the natural behavior of male African cichlid fish (Astatotilapia burtoni), to determine if they could be trained on a spatial task to gain access to females and shelter. We measured both how successfully animals completed this task over time and whether and how immediate early gene and hormone expression profiles were related to success. While training fish in a maze, we measured time to task completion, circulating levels of three key hormones (cortisol, 11-ketotestosterone, and testosterone) and mRNA abundance of seven target genes including three immediate early genes (that served proxies for brain activity) in nine brain regions. Data from our subjects fell naturally into three phenotypes: fish that could be trained (learners), fish that could not be trained (non-learners) and fish that never attempted the task (non-attempters). Learners and non-learners had lower levels of circulating cortisol compared to fish that never attempted the task. Learners had the highest immediate early gene mRNA levels in the homologue of the hippocampus (dorsolateral telencephalon; Dl), lower cortisol (stress) levels and were more motivated to accomplish the task as measured by behavioral observations. Fish that never attempted the task showed the lowest activity within the Dl, high stress levels and little to no apparent motivation. Data from non-learners fell between these two extremes in behavior, stress, and motivation.
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