Transient local adaptation and source-sink dynamics in experimental populations experiencing spatially heterogeneous environments

Local adaptation is determined by the strength of selection and the level of gene flow within heterogeneous landscapes. The presence of benign habitat can act as an evolutionary stepping stone for local adaptation to challenging environments by providing the necessary genetic variation. At the same time, migration load from benign habitats will hinder adaptation. In a community context, interspecific competition is expected to select against maladapted migrants, hence reducing migration load and facilitating adaptation. As the interplay between competition and spatial heterogeneity on the joint ecological and evolutionary dynamics of populations is poorly understood, we performed an evolutionary experiment using the herbivore spider mite Tetranychus urticae as a model. We studied the species's demography and local adaptation in a challenging environment that consisted of an initial sink (pepper plants) and/or a more benign environment (cucumber plants). Half of the experimental populations were exposed to a competitor, the congeneric T. ludeni. We show that while spider mites only adapted to the challenging pepper environment when it was spatially interspersed with benign cucumber habitat, this adaptation was only temporary and disappeared when the populations in the benign cucumber environment were expanding and spilling-over to the challenging pepper environment. Although the focal species outcompeted the competitor after about two months, a negative effect of competition on the focal species's performance persisted in the benign environment. Adaptation to challenging habitat in heterogeneous landscapes thus highly depends on demography and source-sink dynamics, but also on competitive interactions with other species, even if they are only present for a short time span.