Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands

Phenotypic plasticity enables a single genotype to produce multiple phenotypes in response to environmental variation. Plasticity may play a critical role in the colonization of novel environments, but its role in adaptive evolution is controversial. Here we suggest that rapid parallel regulatory adaptation of Anolis lizards to urban heat islands is due primarily to selection for reduced and/or reversed heat-induced plasticity that is maladaptive in urban thermal conditions. We identify evidence for polygenic selection across genes of the skeletal muscle transcriptome associated with heat tolerance. Forest lizards raised in common garden conditions exhibit heat-induced changes in expression of these genes that largely correlate with decreased heat tolerance, consistent with maladaptive regulatory response to high-temperature environments. In contrast, urban lizards display reduced gene expression plasticity after heat challenge in common garden and a significant increase in gene expression change that is congruent with greater heat tolerance, a putatively adaptive state in warmer urban environments. Genes displaying maladaptive heat-induced plasticity repeatedly show greater genetic divergence between urban and forest habitats than those displaying adaptive plasticity. These results highlight the role of selection against maladaptive regulatory plasticity during rapid adaptive modification of complex systems in the wild.