Selection often operates not directly on phenotypic traits but on performance which is important as several traits may contribute to a single performance measure (many‐to‐one mapping). Although largely ignored in the context of selection, this asks for studies that link all relevant phenotypes with performance and fitness. In an enclosure experiment, we studied links between phenotypic traits, swimming performance and survival in two Enallagma damselflies. Predatory dragonflies imposed survival selection for increased swimming propensity and speed only in E. annexum; probably E. aspersum was buffered by the former species’ presence. Accordingly, more circular caudal lamellae, structures involved in generating thrust while swimming, were selected for only in E. annexum. Other phenotypic traits that contributed to swimming speed were apparently not under selection, probably because of many‐to‐one mapping (functional redundancy). Our results indicate that not only the phenotypic distributions of syntopic prey organisms but also many‐to‐one mapping should be considered when documenting phenotype–performance–fitness relationships.

Optimality models predict that, under a time constraint, organisms should accelerate development, and preferably so by increasing growth rate, to keep size at emergence constant. Unfortunately, most tests did neglect genetic constraints and interchanged mass with body size which may explain mixed support for some of the models' predictions. We imposed time constraints on full sibling larvae of the damselfly Enallagma cyathigerum by manipulating day length regimes. Under a time constraint, larval development and growth rate based on size indeed were faster. This made it possible to keep size at emergence constant, despite the shorter development time. Interestingly, under a time constraint, growth rate based on mass was not increased and larvae had a lower mass at emergence. We see two reasons for this difference between body mass and size. First, size is fixed at emergence, while mass can still increase in many insects. Secondly, genetic constraints may have contributed to different responses for size and mass. In general, our results strongly suggest discriminating between size and mass when testing life history responses.

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Summary1. In contrast to other phenotypic traits, selection on physiological traits remains largely undocumented. We have evaluated survival selection imposed by predation by dragonflies on the activity of arginine kinase (Ak), a key enzyme delivering energy for escape performance in invertebrates. 2. To accomplish this, we conducted a semi-natural field enclosure experiment in which we manipulated predation by large dragonfly predators, and quantified escape swimming speed and Ak in the prey, the damselfly Enallagma vesperum. To avoid confounding selection on Ak with selection on other swimming speed-related variables, we also scored all morphological and behavioural traits thought to underlie swimming speed in these damselflies. 3. Dragonfly predators imposed considerable mortality and selected for faster swimming speed and higher activity levels of Ak. Furthermore, higher Ak levels contributed to higher swimming speeds, confirming the mechanistic role of Ak for escape performance. Although morphological (size of the caudal lamellae which generate trust) and behavioural (number of beats made by the abdomen during swimming and the start angle of the C-start) variables contribute to increasing swimming speed, we detected no selection on these variables. This may be due to functional redundancy. 4. Taken together, our results indicated selection on Ak and suggested that selection on physiological traits may be as strong as selection on morphology and life history traits.

Despite the many study systems where predation has played a major role in phenotypic diversification and speciation, the underlying selective regimes imposed by different predator assemblages have rarely been quantified. We did so for the damselfly genus Enallagma that strongly diverged in anti-predator traits when the ancestral species occupying lakes containing fish (hereafter fish lakes) repeatedly invaded fishless lakes with dragonfly larvae as top predators (hereafter dragonfly lakes). In two selection experiments in field enclosures we quantified the selection on two key escape traits of two fish-lake Enallagma species associated with survival selection by fish in the ancestral fish lakes and by dragonfly predators in the invaded fishless, dragonfly lakes. In accordance with the different hunting modes, fish imposed selection for a decreased swimming propensity while dragonfly larvae imposed selection for increased swimming speed in one of the two species. In two complementary quantitative genetic rearing experiments we found relatively low but significant broad-sense heritabilities for both escape traits. Integrating these estimates for the selection coefficients and the heritabilities, suggests that the evolutionary increase in swimming speed associated with the habitat shift may have occurred rapidly. Our study suggests that the phenotypic evolution of ecologically important traits related to habitat shifts may occur at an ecological timescale.