In the 1940s, C. H. Waddington discovered a peculiar phenomenon in fruit flies: traits could appear in response to environmental stress in an individual’s lifetime and then be passed down to future generations. Waddington proposed that this wasn’t the inheritance of acquired traits, but actually due to pre-existing genetic variation that had no effect until the flies were stressed. In the August issue of GENETICS, Fanti and Piacentini et al. revisit Waddington’s famous experiments with modern sequencing technology to show that this phenomenon can also be driven by newly arising DNA mutations.
The authors followed Waddington’s fairly simple experimental framework: take flies from natural populations and expose them to high temperatures for a short time during pupation. Observe the adult phenotypes, and then do it all again the next generation. Repeat this process until strange phenotypes emerge following the heat shock treatment.
The authors focused on four phenotypes caused by well-studied mutations in fruit flies, including sepia eye color and forked bristle mutations. These phenotypes began to appear after heat shock treatment between four and twelve generations after the experiment began. The scientists then selected for a phenotype by crossing the flies displaying it. They repeated this procedure until the phenotypes appeared not only after heat stress but were stably maintained in regular conditions.
They confirmed the presence of genetic mutations in the heat shocked mutant stocks using DNA sequencing. In the fixed mutant stocks, they found clear genetic causes of the mutant phenotypes. In two cases, a deletion mutation disrupted the protein coding sequence, and the other two genes carried transposable element insertions. None of the mutations were present in the genomes of the parental flies; these mutations were new, arising during the course of the experiment. Clearly, they were what allowed the phenotypes to be maintained stably without heat stress.
These results show that Waddington was wrong: inheritance of the abnormal post-heat shock phenotypes was not due to cryptic variation present in the parent lines. A different mechanism must be responsible. Heat shock stress may cause double-stranded DNA breaks, which can lead to deletions like the ones observed here. It may also activate transposable elements since the authors found higher levels of transposable element transcripts in flies that had been heat shocked.
But how could these new mutations appear in the same genes that were initially disabled by heat shock? How can a stress-dependent phenotype become genetically encoded? The authors suggest epigenetic changes may be involved. Heat stress could result in epigenetic alteration of particular loci to change their expression, leading to the observed heat-dependent phenotypes. This same epigenetic activity may make this stretch of DNA more susceptible to mutation, which could be very likely in the face of heat shock-induced double-stranded breaks or activated transposable elements.
If this model holds true, it could have serious evolutionary implications. In the wild, plastic traits like these post-heat shock phenotypes are often adaptive and help organisms survive in difficult, changing environments. It has been proposed that under natural selection such environmentally-induced traits can eventually become genetically encoded. Called the Baldwin Effect, this process illustrates how heritable behaviors like the human capacity for language might evolve. The results of this study provide a viable mechanism for this powerful evolutionary phenomenon.
CITATION
Canalization by Selection of de Novo Induced Mutations
Katie is a science writer at GSA. She did her PhD work on the evolutionary consequences of genetic conflict in fruit flies at the University of Georgia.
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