The evolutionary advantage of heritable phenotypic heterogeneity
Oana Carja, Joshua B Plotkin
Abstract:
Phenotypic plasticity is an evolutionary driving force in diverse
biological processes, including the adaptive immune system, the
development of neoplasms, and the bacterial acquisition of drug
resistance. It is essential, therefore, to understand the evolutionary
advantage of an allele that confers cells the ability to express a range
of phenotypes. Of particular importance is to understand how this
advantage of phenotypic plasticity depends on the degree of heritability
of non-genetically encoded phenotypes between generations, which can
induce irreversible evolutionary changes in the population. Here, we
study the fate of a new mutation that allows the expression of multiple
phenotypic states, introduced into a finite population otherwise
composed of individuals who can express only a single phenotype. We
analyze the fixation probability of such an allele as a function of the
strength of inter-generational phenotypic heritability, called memory,
the variance of expressible phenotypes, the rate of environmental
changes, and the population size. We find that the fate of a
phenotypically plastic allele depends fundamentally on the environmental
regime. In a constant environment, the fixation probability of a
plastic allele always increases with the degree of phenotypic memory.
In periodically fluctuating environments, by contrast, there is an
optimum phenotypic memory that maximizes the probability of the plastic
allele's fixation. This same optimum value of phenotypic memory also
maximizes geometric mean fitness, in steady state. We interpret these
results in the context of previous studies in an infinite-population
framework. We also discuss the implications of our results for the
design of therapies that can overcome resistance, in a variety of
diseases.
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