Addressing multi-generational non-genetic inheritance 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 fitness can recover by adaptive genetic evolution over multiple generations, but their immediate responses often involve non-genetic mechanisms. When such non-genetic responses have dynamics that span multiple generations, their effects at the population level can be difficult to distinguish from those of evolution by selection of genetic variants. While the existence of non-genetic inheritance is no longer controversial, we here argue that its potential contribution to observed patterns in evolutionary studies is still largely overlooked, especially regarding processes that unfold over multiple generations, which we call multigenerational non-genetic inheritance (MUNGI). We highlight three major forms of MUNGI that should be particularly problematic if not properly accounted for: delayed impact of stress, transgenerational plasticity, and priming. We summarize how each may impact the dynamics of observed phenotypic change across generations in concrete experimental contexts (e.g., experimental evolution, common gardens, ecotoxicological experiments, dose-response assays). We propose that analysing the dynamic properties (rate, stability, reversibility, etc.) of MUNGI processes, as well as 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 novel or changing environments.