Managing the tradeoff between reproduction and survival requires flexibility in behaviour and gene regulation in three-spined stickleback.

Abstract

Predators exert a powerful selective force, however, predator avoidance can conflict with other important activities such as attracting mates. Decisions over whether to court mates versus avoiding predators are vital to fitness, yet the mechanistic underpinnings of how animals manage such tradeoffs are poorly understood. Here, we investigate the flexibility of behaviour and gene regulation in response to a tradeoff between avoiding predators (survival) and courting potential mates (reproduction) in three-spined stickleback (Gasterosteus aculeatus). We compared behavioural and transcriptomic responses of male sticklebacks faced with a courtship opportunity and cues of a predator simultaneously with the responses of males faced with a courtship opportunity or cues of a predator alone, and found that males behaviourally compromised courtship in favour of predator avoidance when faced with a tradeoff between them. The need to manage this tradeoff elicited dynamic changes in brain gene expression, and sets of functionally connected genes were organized into discrete modules based on co-expression. Additionally, we found that behavioural flexibility in response to tradeoffs corresponded to flexibility in gene regulatory network structure. Combined, these results uncover the coordinated response by the brain to a fundamental ecological tradeoff, providing insight into the structure and function of genetic networks underpinning how animals make fitness-influencing decisions.