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Transgenerational phenotypic plasticity is a rapid, non-genetic response to environmental changes. It can mitigate the effects of environmental stresses on populations. However, little is known about the evolution of this plasticity in the absence of genetic variation although several non-genetic inheritance mechanisms have been identified as epigenetic inheritance (ie, vertical transmission of epigenetic marks such as methylation of DNA that influence gene expression) or cultural.

Aphids against ladybugs

When aphids are attacked by predators such as ladybugs, they produce winged offspring by clonal reproduction (parthenogenesis). The production of winged offspring in response to predation is therefore an example of transgenerational plasticity since the genotype of winged and non-winged individuals, two very different phenotypes, is the same. This phenotypic variation is essentially due to the fact that the detection of predators by aphids triggers the establishment of complex epigenetic marks that have the effect of profoundly modifying the expression of a large number of genes in the next generation. This process can therefore be considered as a form of epigenetic inheritance, raising the question of its potential role in evolution.

In order to test whether this transmitted epigenetic variation could participate in evolution the authors have therefore used this system to test whether evolution can exist in the absence of any initial genetic diversity. They followed the modifications of this plastic response over 27 generations in the presence or not of predators, and in the absence of initial genetic variation (thanks to the existence of a clonal reproduction allowing to leave a single individual). Note that, unlike the natural environment, in their experimental system, winged aphids were at a disadvantage. It was therefore expected that the tendency to make winged aphids in the presence of predators decreases over the generations.

The researchers found that the frequency of winged aphids increased rapidly in response to predators, and then stabilized at a high level for the next 25 generations of the experiment. They conclude that stable phenotypic reconstruction occurs in each generation when aphids are constantly exposed to predators. To test the persistence of the winged phenotype once the predators were removed, the researchers generated, at three stages of this long history of selection, parallel lines in which they removed the predators. These parallel lines were created at the beginning (generation 3), in the middle (generation 13) and at the end (generation 22) of the experimental evolution. They found that the longer aphids are exposed to predators, the less the winged phenotype persists in the population. As expected, aphids subjected to predation for a long time therefore decreased their ability to produce winged offspring in the presence of predators.

In addition, aphids continuously exposed to predators for 22 generations developed a significantly lower plastic response than aphids never exposed to predators. So the decrease in their ability to produce winged offspring in the presence of predators is at least partly due to a decrease in their plastic response. It seems that this decrease in plasticity is adaptive because in the experimental system it increases the phenotypic aptitude of the aphids.

Their results suggest that the evolution of plasticity can occur in the absence of any initial genetic variation. The authors then discuss the fact that this type of non-genetic inheritance could play an important role in the evolutionary responses to ongoing environmental changes.