The evolution of epigenetically mediated adaptive transgenerational plasticity in a subdivided population

Abstract

Transgenerational plasticity (TGP) occurs when offspring exhibit plasticity in traits induced by the environments experienced by their parents, and represents a nongenetic mechanism of inheritance. Evidence that traits can be transmitted to future generations by means other than genetic inheritance has caused a surge of interest in epigenetic inheritance, but evidence for epigenetic modifications being both adaptive and heritable remains scarce. What features would make a species most prone to evolve a system of epigenetically mediated adaptive TGP? Here, we use population‐genetic models modified to include epigenetic induction and inheritance to investigate if and when epigenetically mediated adaptive TGP would be expected to evolve for a population subdivided between two habitats connected by migration. We show that differences in the direction of selection between the two habitats drives the evolution of epigenetically mediated adaptive TGP. With low migration, the strength of indirect selection in favor of epigenetically mediated adaptive TGP increases with migration rate. Yet, with higher migration, the opposite trend is observed. We predict that species subdivided between habitats that differ in the direction of selection with moderate migration rates between the habitats would be most likely to evolve epigenetically mediated adaptive TGP if costs of producing such systems are not too high.

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

“…If phenotypically-plastic epigenetic marks are advantageous and heritable, then selection might act directly on the repression of these genomic locations, even in a homogenized genetic background, particularly if such genes are metabolically costly and provide no fitness benefit if activated. Such hypotheses align with theoretical models of epigenetically mediated adaptive plasticity, although further empirical investigations in wild populations are merited (Greenspoon & Spencer, 2018). Provided that epigenetic patterns are maintained across generations (Colomé-Tatché et al, 2012;Joo et al, 2018;Liu, Wang, Hu, Wang, & Zhang, 2018;Schmitz et al, 2013), DNA methylation could be integrated into the working model of ecological speciation with gene flow by mediating gene expression and the optimal phenotype under local conditions (Greenspoon & Spencer, 2018).…”

“…As evidence accumulates regarding the mechanisms underlying epigenetic inheritance (Yu, Wang, & Moazed, 2018) and the adaptive benefits of epialleles (He et al, 2018), DNA methylation has the potential to be worked into a framework of adaptive divergence (Greenspoon & Spencer, 2018;Vogt, 2017Vogt, , 2018 and ultimately into the ecological speciation model (Feder et al, 2012). It is possible that the interplay of subtle nuclear divergence and DNA methylation could mediate local adaptation via hypermethylation of locally deleterious genes, although longitudinal common garden or translocation experiments are required to explore this (Dubin et al, 2015;Vilgalys, Rogers, Jolly, Mukherjee, & Tung, 2019).…”

“…Moreover, an aspect of molecular variation that is undetected by standard genetic sequencing involves direct modifications to the structure of DNA. Epigenetic modifications like DNA methylation are influenced by environmental conditions and affect gene expression, and thus could be indicative of early divergence due to local adaptation (Greenspoon & Spencer, ; He et al, ; Vogt, ).…”

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

“…Recent models have shed light into the evolution of transgenerational plasticity in patchy environments (Leimar & McNamara, ), explicitly testing the conditions that favor deterministic versus. randomizing maternal effects (Proulx & Teotonio, ), studying how migration and population structure impact the evolution of transgenerational plasticity (Greenspoon & Spencer, ), determining the optimal levels of epigenetic resetting between generations (Uller, English, & Pen, ), and calculating the interaction between the evolution of within‐generation and transgenerational phenotypic plasticity (Kuijper & Hoyle, ). Additionally, other groups have developed systems comparing invasion probabilities of lines with various epigenetic modifier loci (Furrow & Feldman, ) and applied information theory (Donaldson‐Matasci, Bergstrom, & Lachman, ) to the study of transgenerational phenotypic plasticity.…”

Genome-wide sampling suggests island divergence accompanied by cryptic epigenetic plasticity in Canada lynx

“…It is possible that hypermethylation of locally deleterious genes could provide a precursory mechanism to adaptive divergence over linked SNPs. In contrast, if phenotypically-plastic epigenetic marks are advantageous and heritable, then selection might act directly on the repression of these genomic locations, even in the absence of underlying genetic divergence, particularly if such genes are metabolically costly and provide no fitness benefit, if activated(44). Provided that the mechanisms underlying transgenerational epigenetic inheritance canmaintain methylomic patterning across generations (Colome-Tatche et al 2012, Schmitz et al 2013, Liu et al 2018, Joo et al 2018, but see Kazachenka et al 2018), DNA methylation could be integrated into the working model of ecological speciation with gene flow by mediating gene expression and the optimal phenotype under local conditions.…”