Evolution has since the very beginning resulted in organisms which can sort fitness-related information from noise, evaluate it and respond to it. In animals, the architecture for proximate control of behaviour and physiology has been gradually evolving since before the Cambrian explosion of animal phyla. It integrates many different survival circuits, for example for danger, feeding and reproduction, and operates through reflexes, instincts, homeostatic drives and precursors to human emotions. Although teleost brains differ substantially from the much better understood brains of terrestrial vertebrates, their anatomy, physiology and neurochemistry all point towards a common and malleable architectural template with strong and flexible effects on fish behaviour and elements of personality. We describe the main components of this architecture and its role in fish behaviour from the perspectives of adaptation, evolutionary history and gene pools. Much research is needed, as several of the basic assumptions for architectural control of behaviour and physiology in teleosts are not thoroughly investigated. We think the architecture for behavioural control can be used to change ecosystem models from a bottom-up perspective to also include behaviourally mediated trophic cascades and trait-mediated indirect effects. We also discuss the utility of modelling based on proximate architectural control for fish welfare studies.