Improving our understanding of adaptation to environmental change by addressing multi-generational non-genetic inheritance

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

Populations that face abrupt environmental change reducing their fitness can recover by adaptive genetic evolution over tens to hundreds of generations, but their immediate responses often involve non-genetic mechanisms. When such non-genetic responses span multiple generations, their dynamics may be difficult to distinguish from those of genetic evolution. We here argue that focusing research on such multigenerational non-genetic inheritance (MUNGI) should be crucial to better understand and predict eco-evolutionary responses to environmental stress. We survey the most salient forms of MUNGI (delayed impact of stress, transgenerational plasticity, and priming), with a focus on how they may impact the dynamics of observed phenotypic change across multiple generations in concrete experimental contexts (experimental evolution, common gardens, ecotoxicological experiments, dose-response assays). Analysing the rate, stability, and reversibility of MUNGI, as well as their relative contributions to overall phenotypic responses, and their interactions with genetic changes, should be particularly fruitful towards a more comprehensive deciphering of evolutionary responses to novel or changing environments.