How differing modes of non‐genetic inheritance affect population viability in fluctuating environments

Abstract

Different modes of non‐genetic inheritance are expected to affect population persistence in fluctuating environments. We here analyse Caenorhabditis elegans density‐independent per capita growth rate time series on 36 populations experiencing six controlled sequences of challenging oxygen level fluctuations across 60 generations, and parameterise competing models of non‐genetic inheritance in order to explain observed dynamics. Our analysis shows that phenotypic plasticity and anticipatory maternal effects are sufficient to explain growth rate dynamics, but that a carryover model where ‘epigenetic’ memory is imperfectly transmitted and might be reset at each generation is a better fit to the data. We further find that this epigenetic memory is asymmetric since it is kept for longer when populations are exposed to the more challenging environment. Our analysis suggests that population persistence in fluctuating environments depends on the non‐genetic inheritance of phenotypes whose expression is regulated across multiple generations.

Reduced phenotypic plasticity evolves in less predictable environments

“…Indeed these changes consist not only of trends in mean environments, but also alterations in the magnitude and predictability of natural environmental fluctuations (Wigley et al ., 1998; Boer, 2009). Theoretical work has made it clear that phenotypic plasticity can strongly influence extinction risk in response to changing environmental predictability (Reed et al ., 2010; Chevin et al ., 2013a; Botero et al ., 2015; Ashander et al ., 2016), which was recently confirmed empirically using laboratory experiments (Proulx et al ., 2019; Rescan et al ., 2020). In particular, this theory has shown that evolution of lower phenotypic plasticity can reduce extinction risk under reduced environmental predictability, by decreasing the magnitude of mismatches between the population mean phenotype and the optimum phenotype determined by the environment (Chevin et al ., 2013a; Ashander et al ., 2016).…”

Ecological divergence of wild strawberry DNA methylation patterns at distinct spatial scales

“…Vice versa, our results suggest that the loss of an epigenetic memory requires long‐term release of stressful conditions, and that multiple generations without stress exposure are required for completely resetting the epigenetic machinery. Multigenerational persistence of epigenetic signatures (i.e., epigenetic carryover) and thus slow transgenerational loss of epigenetic variation is a typical epigenetic mechanism observed in common gardens quantifying epigenetic variation across generations (Miska & Ferguson‐Smith, 2016; Paszkowski & Grossniklaus, 2011; Proulx et al., 2019). Given the natural ubiquity of transgenerational epigenetic inheritance, as indicated by the former studies, at least part of the epigenetic patterns observed in our common garden generation is expected to reflect such epigenetic carryover.…”

Ecological divergence of DNA methylation patterns at distinct spatial scales

“…Multi-generational persistence of epigenetic signatures (i.e. epigenetic carryover) and thus slow trans-generational loss of epigenetic memory is a typical epigenetic mechanism observed in common gardens quantifying epigenetic variation across generations (Paszkowski & Grossniklaus 2011; Miska & Ferguson-Smith 2016; Proulx et al . 2019).…”