Addressing multi-generational non-genetic responses in experimental studies of evolution

Giacomo Zilio, Stéphanie Bedhomme, Emanuel A. Fronhofer, Staffan Jacob, Delphine Legrand, Hervé Philippe, Luis-Miguel Chevin

Populations that face environmental change reducing their mean fitness can recover by adaptive genetic evolution over multiple generations, but their immediate responses may also involve non-genetic mechanisms, though the latter can be difficult to demonstrate. When the dynamics of such non-genetic changes in mean phenotype and fitness span multiple generations, their effects at the population level can be difficult to distinguish from those of natural selection on genetic variants. While the existence of non-genetic inheritance is no longer controversial, we argue that its potential contribution to observed patterns in evolutionary studies remains overlooked, especially for processes leading to phenotypic change that unfolds over multiple generations, which we call multigenerational non-genetic responses (MUNGER). We highlight three major forms of MUNGER that, if not properly accounted for, could confound inference about genetic changes: delayed impact of stress, transgenerational plasticity, and priming. We summarize how each may impact the dynamics of phenotypic change across generations in concrete experimental contexts (e.g., experimental evolution, common gardens, ecotoxicological experiments). We propose that analysing the dynamic properties of MUNGER, their relative contributions to overall phenotypic responses, and how they interact with genetic changes, should help build a more comprehensive understanding of evolutionary responses to changing environments.