Body size, performance and fitness in Galapagos marine iguanas

Complex organismal traits such as body size are influenced by innumerable selective pressures, making the prediction of evolutionary trajectories for those traits difficult. A potentially powerful way to predict fitness in natural systems is to study the composite response of individuals in terms of performance measures, such as foraging or reproductive performance. Once key performance measures are identified in this top-down approach, we can determine the underlying physiological mechanisms and gain predictive power over long-term evolutionary processes. Here we use marine iguanas as a model system where body size differs by more than one order of magnitude between island populations. We identified foraging efficiency as the main performance measure that constrains body size. Mechanistically, foraging performance is determined by food pasture height and the thermal environment, influencing intake and digestion. Stress hormones may be a flexible way of influencing an individual's response to low-food situations that may be caused by high population density, famines, or anthropogenic disturbances like oil spills. Reproductive performance, on the other hand, increases with body size and is mediated by higher survival of larger hatchlings from larger females and increased mating success of larger males. Reproductive performance of males may be adjusted via plastic hormonal feedback mechanisms that allow individuals to assess their social rank annually within the current population size structure. When integrated, these data suggest that reproductive performance favors increased body size (influenced by reproductive hormones), with an overall limit imposed by foraging performance (influenced by stress hormones). Based on our mechanistic understanding of individual performances we predicted an evolutionary increase in maximum body size caused by global warming trends. We support this prediction using specimens collected during 1905. We also show in a common-garden experiment that body size may have a genetic component in iguanids. This 'performance paradigm' allows predictions about adaptive evolution in natural populations.