Growth is an important theme in biology. Physiologists often relate growth rates to hormonal control of essential processes. Ecologists often study growth as a function of gradients or combinations of environmental factors. Fewer studies have investigated the combined effects of environmental and hormonal control on growth. Here, we present an evolutionary optimization model of fish growth that combines internal regulation of growth by hormone levels with the external influence of food availability and predation risk. The model finds a dynamic hormone profile that optimizes fish growth and survival up to 30 cm, and we use the probability of reaching this milestone as a proxy for fitness. The complex web of interrelated hormones and other signalling molecules is simplified to three functions represented by growth hormone, thyroid hormone and orexin. By studying a range from poor to rich environments, we find that the level of food availability in the environment results in different evolutionarily optimal strategies of hormone levels. With more food available, higher levels of hormones are optimal, resulting in higher food intake, standard metabolism and growth. By using this fitnessbased approach we also find a consequence of evolutionary optimization of survival on optimal hormone use. Where foraging is risky, the thyroid hormone can be used strategically to increase metabolic potential and the chance of escaping from predators. By comparing model results to empirical observations, many mechanisms can be recognized, for instance a change in pace-oflife due to resource availability, and reduced emphasis on reserves in more stable environments. This article has an associated First Person interview with the first author of the paper.

Growth is an important theme in many biological disciplines. Physiologists often relate growth rates to hormonal control of essential processes. Ecologists often study growth as function of gradients or combinations of environmental factors. Fewer studies have investigated the combined effects of environmental and hormonal control on growth. Here, we present an evolutionary optimization model of fish growth that combines internal regulation of growth by hormone levels with the external influence of food availability and predation risk. Hormones are represented by growth hormone, thyroid hormone and orexin functions. By studying a range from poor to rich environments, we find that the level of food availability in the environment results in different evolutionarily optimal strategies of hormone levels. With more food available, higher levels of hormones are optimal, resulting in higher food uptake and growth. By using this fitness-based approach we also find a consequence of evolutionary optimization of survival on optimal hormone use. Where foraging is risky, aerobic scope can be used strategically to increase the chance of escaping from predators. By comparing model results to empirical observations, many mechanisms can be recognized, for instance a change in pace-of-life due to resource availability, and reduced emphasis on reserves in more stable environments. Summary statement We combine physiological, environmental and evolutionary aspects of fish growth in a state-dependent model where the optimal regulation of growth and survival is achieved through hormonal regulation of behaviour.

Evolutionary ecology often studies how environmental factors define optimal phenotypes without considering the bodily mechanisms involved in their regulation. Here we used a dynamic optimisation model to investigate optimally concerted hormonal control of the phenotype. We studied a semi-realistic situation where hormonal control of appetite, metabolism and growth acts to prepare juvenile fish for an uncertain future with regard to food availability. We found a bottom-up effect in that hormone levels varied across environments and affected a range of phenotypic changes. We also describe a top-down effect as natural selection varied across environments, which affected evolutionary optimisation of hormone levels. These combined top-down and bottom-up effects produced a hormone-regulated phenotype that adjusted its foraging intensity and risk-taking in adaptive ways depending on the differences between current and expected long-term environmental conditions. Hence, understanding the response of these fish to their current conditions also requires an understanding of their future expectations. We found that when food availability was low, it was optimal for the juvenile fish to have low growth hormone, thyroid hormone and orexin levels, contrary to when food availability was high when these levels were higher. Individual variation emerged from the individually experienced food availability trajectories: Those that on average experienced higher food availability grew faster and had higher short-term mortality risk. They also had higher survival probability throughout the growth period. The opposite was true for individuals experiencing lower food availability. Hormonal mechanisms that often are overlooked by ecologists are thus important in the ultimate adaptive control of both behaviour and physiology, thereby impacting fitness through growth and survival.

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Using a dynamic optimisation model for juvenile fish in stochastic food environments, we investigate optimal hormonal regulation, energy allocation and foraging behaviour of a growing host infected by a parasite that only incurs an energetic cost. We find it optimal for the infected host to have higher levels of orexin, growth- and thyroid hormones, resulting in higher activity levels, increased foraging, and faster growth. This growth strategy thus displays several of the fingerprints often associated with parasite manipulation: higher levels of metabolic hormones, faster growth, higher allocation to reserves (i.e. parasite-induced gigantism), higher risk taking and eventually higher predation rate. However, there is no route for manipulation in our model, so these changes reflect adaptive host compensatory responses. Interestingly, several of these changes also increase the fitness of the parasite. Our results call for caution when interpreting observations of gigantism or risky host behaviours as parasite manipulation without further testing.