Modelling Selection under Soft Inheritance

Abstract

Epigenetic modifications to the genome, altering gene expression without changing the DNA sequence, can lead to changes to an individual’s phenotype. Furthermore, these changes to gene expression can be passed from one generation to the next through stable inheritance of epigenetically modifiable alleles (epialleles). Indeed, empirical studies have shown that epigenetic marks can be inherited with high fidelity between generations in many plant and animal model species. Moreover, epigenetic phenomena have been observed in natural populations, including humans. Although the effects of ‘gene-environment’ interactions have been widely acknowledged for some time, some theorists have dismissed the broader evolutionary significance of this type of non-genomic inheritance system. Consequently, the population-level consequences of transgenerational epigenetic inheritance have, until recently, been largely ignored. This thesis makes a start towards remedying this omission by integrating the complex nature of epigenetics into standard genetic models of constant viability selection.

After setting out a review of the relevant literature in Chapter One, Chapter Two introduces two simple population-epigenetic models. These models consider how two diverse environmental cues, each capable of inducing epigenetic change, can influence the frequency of one or more epialleles under selection. A fundamental aim of this Chapter is to investigate the effect of varying rates at which epialleles resist environmental influences (maintaining their original epigenetic status, thus being inherited, unchanged, transgenerationally) on the dynamics of the population. Next, in Chapter Three, we expand on the simple population-epigenetic models presented in Chapter Two by providing for different levels of epigenetic resetting, thereby increasing epigenetic diversity and resulting in multiple epigenetic states among genetically identical individuals. We show that both epigenetic resetting and the frequency of environmental cues that induce epigenetic change are crucial parameters for maintaining phenotypic variation through epialleles. We then model a similar type of epigenetic inheritance system – paramutation – in which a meiotically heritable change in gene expression is caused by an interaction between homologous alleles. We demonstrate in Chapter Four that paramutation can create long-term biological diversity in the absence of genetic change, and even in the absence of the original paramutagenic allele. Finally, in Chapter Five, we consider whether an initially monomorphic population in two different environments can be invaded by an epigenetically modifiable allele. This model provides that the allele initially fixed in the population is insensitive to the environmental cues to which it is exposed. In contrast, the invading allele is susceptible to epigenetic modification upon exposure to environmental influences, resulting in two distinct epiallelic variants that code for different phenotypic traits in each environment.

Overall, these models reveal how transgenerational epigenetic inheritance has the potential to profoundly affect the outcome of selection, resulting in elevated levels of phenotypic variation for a wide variety of parameters. We conclude that attributing evolution to only a traditional genetic model may fail to encompass the broad scope of phenotypic differences observed in nature.