Epigenetic Adaptation to Changing Environments

Accumulated evidence of transgenerational inheritance of epigenetic and symbiotic changes begs

the question of whether (and under which conditions) the population can benefit from inheritance

of changes that are acquired during the individuals’ lifetime. To address this question, we introduce

a population epigenetics model of individuals undergoing stochastic and/or induced changes that

are either partially or fully transmitted to the offspring. This model is equally applicable to internal

changes in individuals (e.g. epigenetic and symbiotic variations) as well as niche construction

changes that they make in their environment. Potentially adaptive and maladaptive responses are

represented, respectively, by induced changes that reduce and increase the individuals’ rate of death

(i.e. reduction and increase of selective pressure). We use this framework to investigate how inheritance

of acquired changes affects the long-term dynamics of the population. Analytic solution in a

simple case of a population exposed to environments that change in time shows that inheritance of

changes that transiently alleviate the selective pressure is beneficial even when the offspring environment

differs from that of their parents. The benefit from these changes is even more pronounced

at lower fidelity of inheritance as well as for populations with age-dependent decline in fertility.

We also show that this benefit is essential for preventing population extinction under a range of

successive shifts in the environment. Analysis of long-term influences of various population and

environmental factors reveals a non-trivial landscape of outcomes, including a surprising regime in

which the population benefits from inheritance of changes that increase the selective pressure. Taken

together, these findings show that inheritance of changes that are dynamically acquired within a

generation can have a tremendous benefit for the evolution of the population on timescales that are

much longer than the lifetime of an individual.