Cryptic genetic variation and its contribution to genetic assimilation in natural populations of Drosophila melanogaster

Abstract

Over 65 years ago, Waddington demonstrated phenotypically plastic traits can evolve to become constitutive, a process he termed genetic assimilation. Experiments demonstrated genetic assimilation evolves rapidly, with the response in large part due to segregating genetic variation only expressed in rare/novel environments, but otherwise phenotypically cryptic. Despite previous work suggesting a substantial role of cryptic genetic variation contributing to the evolution of genetic assimilation, some have argued for a prominent role for new mutations of large effect concurrent with selection. Less concerned by the relative contribution of CGV or new variants, Waddington aimed to test the role of canalization, an evolved form of robustness. While canalization has been extensively studied, its role in the evolution of genetic assimilation is disputed, in part because explicit tests of evolved robustness are lacking. To address these questions, we recreated Waddington’s selection experiments on an environmentally sensitive change in Drosophila wing morphology (crossvein development), using many independently evolved replicate lineages. Using these we show that 1) CGV has potentially pleiotropic and fitness consequences in natural populations and may not be always be “cryptic”. 2) CGV, but not new variants of large effect are largely responsible for the evolved response demonstrated using both genomic and genetic approaches. 3) Using both environmental manipulations and mutagenesis of the evolved lineages that there is no evidence for evolved changes in canalization contributing to genetic assimilation.