Reexamining Waddington: Canalization and new mutations are not required for the evolution of genetic assimilation
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AbstractOver 65 years ago, Waddington demonstrated ancestrally phenotypically plastic traits can evolve to become constitutive, a process he termed genetic assimilation. Genetic assimilation evolves rapidly, assumed to be 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. Interestingly, Waddington was less concerned by the relative contribution of CGV or new variants, but 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) a polygenic CGV, but not new variants of large effect are largely responsible for the evolved response demonstrated using both genomic and genetic approaches. 2) Using both environmental manipulations and mutagenesis of the evolved lineages that there is no evidence for evolved changes in canalization contributing to genetic assimilation. Finally, we demonstrate that 3) CGV has potentially pleiotropic and fitness consequences in natural populations and may not be entirely “cryptic”.
