When is incomplete epigenetic resetting in germ cells favoured by natural selection?

Abstract

Resetting of epigenetic marks, such as DNA methylation, in germ cells or early embryos is not always complete. Epigenetic states may therefore persist, decay or accumulate across generations. In spite of mounting empirical evidence for incomplete resetting, it is currently poorly understood whether it simply reflects stochastic noise or plays an adaptive role in phenotype determination. Here, we use a simple model to show that incomplete resetting can be adaptive in heterogeneous environments. Transmission of acquired epigenetic states prevents mismatched phenotypes when the environment changes infrequently relative to generation time and when maternal and environmental cues are unreliable. We discuss how these results may help to interpret the emerging data on transgenerational epigenetic inheritance in plants and animals.

Epigenetics in natural animal populations

“…A possible explanation is the hypothetical 'transgenerational washout' epigenetic effect (Burggren, 2015), where the level of epigenetically caused phenotypic modification, in this case reduced lifespan and heat stress resistance, progressively declines across generations to subdetectable levels. This decline may result from rapid adaptation caused by switching between epigenetic variants in periodic environments, as indicated by recent models (Furrow & Feldman, 2014;Uller et al, 2015;Kuijper & Johnstone, 2016).…”

“…In the first approach, the main aim is to investigate the effects of stable levels of epigenetic mutation on the maintenance of genetic or phenotypic variation (P al, 1998;P al & Miklos, 1999;Day & Bonduriansky, 2011;Carja & Feldman, 2012;Geoghegan & Spencer, 2012, 2013Klironomos et al, 2013;Kronholm & Collins, 2015;Day, 2016). In the second approach, the switching rate of epigenetic variation between generations has been identified as an evolutionary variable, which can evolve in response to different environments without interacting with genotypes (Jablonka et al, 1995;Lachmann & Jablonka, 1996;Salath e et al, 2009;Feinberg & Irizarry, 2010;Furrow & Feldman, 2014;Uller et al, 2015;Kuijper & Johnstone, 2016; Table 2). In general, models of epigenetic switching rates have concluded that the rate of temporal environmental change is a key factor controlling epigenetic variation.…”

DNA methylation mediates genetic variation for adaptive transgenerational plasticity

“…More broadly, genetic differences in the expression of within-versus transgenerational plasticity may derive from differences among source populations in historical exposure to particular regimes of environmental change [80]. Recent theory predicts that adaptive within-generation responses will evolve when there is high temporal environmental variability, whereas adaptive transgenerational plasticity is likely to evolve when environments are stable over generations such that parents and offspring experience similar conditions [81,82] (for an empirical example, see [10]). …”

Local adaptation in transgenerational responses to predators

“…In particular, within-generation plasticity is favoured when there exists high temporal variability in the environment, whereas low temporal variability and a slow rate of environmental change are predicted to favour across-generation responses (figure 1) [25]. This is because strong transgenerational responses allow parent and offspring phenotypes to be matched to current conditions when the environment changes infrequently relative to the generation time of the organism [26]. Such a scenario leads to an 'antagonistic' trajectory of evolution whereby divergent patterns of selection favour withinor across-generation plasticity but not both (figure 1).…”

“…That is, within-and across-generation responses will respond in a similar fashion to environmental signals to improve fitness. Only recently, however, has theory identified the ecological selective pressures that may act independently on within-and across-generation responses [25][26][27]. In particular, within-generation plasticity is favoured when there exists high temporal variability in the environment, whereas low temporal variability and a slow rate of environmental change are predicted to favour across-generation responses (figure 1) [25].…”