Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata)

The empirical study of natural selection reveals that adaptations often involve trade-offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life-history evolution on locomotor performance in the live-bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast-start swimming performance to evade predators. Because embryo development increases a female's wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast-start performance. We find evidence for adaptive but constrained evolution of fast-start swimming performance in laboratory trials conducted on second-generation lab-reared fish. Female guppies from high-predation localities attain a faster acceleration and velocity and travel a greater distance during fast-start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high- and low-predation populations. This functional trade-off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole-organism level.