Redesigning the genetic architecture of phenotypically plastic traits in a changing environment

Normal development depends on specific genetic and environmental inputs. When environments change, entire populations of organisms may simultaneously express maladaptive phenotypes. Selection in the new environment may gradually restore the ancestral phenotype by favouring alleles that counteract the environmental perturbation. This evolutionary process is called genetic compensation, and its effect on the fate of novel phenotypes is opposite to that of genetic assimilation. When genetic compensation occurs along a spatial environmental gradient, it results in the geographic pattern known as countergradient variation. Another place to look for genetic compensation is where human activities are causing environmental changes that affect how traits develop. For example, pollutants with endocrine-disrupting effects are altering the reproductive behaviour of natural populations of animals. If such pollutants persist long enough for genetic compensation to occur, the animals may come to depend on the presence of these chemicals for normal development. Taking genetic compensation into account could enhance our understanding of the role of behaviour in evolution in at least three ways: first, behavioural interactions are often the source of selection against environmentally induced phenotypes; second, behavioural traits themselves may often be targets of genetic compensation; and third, behavioural plasticity can delay or prevent genetic compensation. I present examples to illustrate each of these points, and further explore the ramifications of this understudied and underappreciated evolutionary process. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 276–286.