The role of non-genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps

Abstract

Rapid environmental change is predicted to compromise population survival, and the resulting strong selective pressure can erode genetic variation, making evolutionary rescue unlikely. Non-genetic inheritance may provide a solution to this problem and help explain the current lack of fit between purely genetic evolutionary models and empirical data. We hypothesize that epigenetic modifications can facilitate evolutionary rescue through 'epigenetic buffering'. By facilitating the inheritance of novel phenotypic variants that are generated by environmental change-a strategy we call 'heritable bet hedging'-epigenetic modifications could maintain and increase the evolutionary potential of a population. This process may facilitate genetic adaptation by preserving existing genetic variation, releasing cryptic genetic variation and/or facilitating mutations in functional loci. Although we show that examples of non-genetic inheritance are often maladaptive in the short term, accounting for phenotypic variance and non-adaptive plasticity may reveal important evolutionary implications over longer time scales. We also discuss the possibility that maladaptive epigenetic responses may be due to 'epigenetic traps', whereby evolutionarily novel factors (e.g. endocrine disruptors) hack into the existing epigenetic machinery. We stress that more ecologically relevant work on transgenerational epigenetic inheritance is required. Researchers conducting studies on transgenerational environmental effects should report measures of phenotypic variance, so that the possibility of both bet hedging and heritable bet hedging can be assessed. Future empirical and theoretical work is required to assess the relative importance of genetic and epigenetic variation, and their interaction, for evolutionary rescue.

Keywords: climate change; epimutation; evolutionary tracking; evolutionary traps; plasticity; transgenerational epigenetic inheritance.

Figure 1.

Three different ways in which epigenetic modification can increase heritable phenotypic variation and thus evolutionary potential. Red arrows indicate transient nature of these effects

Figure 2.

Epigenetic mechanisms can lead to heritable bet hedging that buffers populations from extinction. ( A ) A population experiences stochastic environmental variation across generations (black solid line) that falls within the zone experienced by the population over its evolutionary history (dotted black line). This is contrasted with directional stochastic variation (solid red line) caused by a rapid environmental shift across the generations that drives the population mean environment beyond normal environmental variation. For example, considering temperature, while we might assume that temperature fluctuations remain constant over time (i.e. they vary randomly within ±3°) the mean temperature might move from 23°C to 25°C over 10 years (what we consider directional stochastic variation). Populations can be maintained through bet hedging strategies within the dotted black lines, but require the presence of heritable phenotypic variation to cope with novel directional environmental changes (red dotted lines). ( B ) A bet hedging strategy fails to allow populations to cope with directional stochastic environmental change (red solid line). Bet hedging results in plastic allocation strategies (e.g. maternal effects) in the parental generation that leads to increased phenotypic variation in the subsequent generation. Selection favours individuals most closely matching the environmental optimum at the time of selection (black square) while selecting against individuals too far from the phenotypic optimum (red square with red X). The next generation, however, will on average exhibit similar phenotypes to generation 5, because these plastic responses are not heritable. ( C ) A bet hedging strategy where phenotypic variation is heritable (heritable bet hedging) allows a population to adaptively track an environmental optimum outside the range experienced in its evolutionary history. This is achieved by recruiting epigenetic mechanisms to ‘convert’ non-heritable phenotypic variability, generated through a bet hedging strategy, to heritable phenotypic variability (i.e. adaptive epigenetic tracking). In both (B) and (C) similar coloured circles (blue or orange) represent the phenotypes of two family lineages while different patterned circles represent each unique generation. Two columns of circles within a given generation represent the phenotypes before selection and the phenotypes left after selection (i.e. circles within the black square). Only 3–4 generations are shown for simplicity

Figure 3.

( A ) Epigenetic buffering helps retain genetic variance in response to a rapid decline in population fitness (dotted line). In response to an environmental stressor, we predict that total phenotypic variance should increase. In F ₁ , intergenerational non-genetic/epigenetic effects (i.e. bet hedging) initially generate most phenotypic variance (orange bar), which shelters genetic variance (black bar) because this process dissociates the genotype from phenotype. In F ₂ , phenotypic variation continues to increase, but a larger proportion of variance is attributed to transgenerational epigenetic inheritance, facilitating the heritability of a portion of the phenotypic variants. Over longer time scales, if the population remains in a stressful environment, it might begin to re-acquire genetic variants (replenishing genetic variance) through biased mutation rates (or through increased rates of mutation). Over longer time periods, we may get genetic assimilation as the population converges on the new fitness optima. ( B ) Depletion of genetic variation in a population when transgenerational epigenetic mechanisms (red bar) comprise a very low, non-significant proportion of the total phenotypic variance. In response to an environmental stressor, we see strong selection on phenotypic variation that slowly depletes genetic variation