Sensitive periods, but not critical periods, evolve in a fluctuating environment: a model of incremental development.

Nicole Walasek,Karthik Panchanathan,Willem E Frankenhuis

doi:10.1098/rspb.2021.2623

Abstract

Sensitive periods, during which the impact of experience on phenotype is larger than in other periods, exist in all classes of organisms, yet little is known about their evolution. Recent mathematical modelling has explored the conditions in which natural selection favours sensitive periods. These models have assumed that the environment is stable across ontogeny or that organisms can develop phenotypes instantaneously at any age. Neither assumption generally holds. Here, we present a model in which organisms gradually tailor their phenotypes to an environment that fluctuates across ontogeny, while receiving cost-free, imperfect cues to the current environmental state. We vary the rate of environmental change, the reliability of cues and the duration of adulthood relative to ontogeny. We use stochastic dynamic programming to compute optimal policies. From these policies, we simulate levels of plasticity across ontogeny and obtain mature phenotypes. Our results show that sensitive periods can occur at the onset, midway through and even towards the end of ontogeny. In contrast with models assuming stable environments, organisms always retain residual plasticity late in ontogeny. We conclude that critical periods, after which plasticity is zero, are unlikely to be favoured in environments that fluctuate across ontogeny.

Highlights

Phenotypic plasticity—the capacity of a single genotype to produce multiple phenotypes depending on environmental and somatic conditions—is widespread in nature [1,2,3]
There is well-established theory exploring the conditions in which phenotypic plasticity is favoured by natural selection over non-plastic development
Plasticity is likely to be favoured when the environment changes between generations at a rate too fast for genetic evolution to track, but slowly enough within generations for organisms to benefit from using early experience to guide phenotypic development [4,5,6]

Summary

Introduction

Phenotypic plasticity—the capacity of a single genotype to produce multiple phenotypes depending on environmental and somatic conditions—is widespread in nature [1,2,3]. Organisms sample imperfect cues to the current environmental state and adjust their phenotypes to maximize survival and reproduction across ontogeny. We use stochastic dynamic programming to compute optimal policies for a range of environments, varying the rate of environmental fluctuations, the reliability of cues, and how long adulthood lasts relative to ontogeny These policies specify the optimal decision for each possible state of an organism, depending on its current phenotype and cues sampled. The algorithm uses the posterior probabilities at the end of ontogeny and the expected fitness across adulthood as a starting point to determine the optimal decision in the final time period and works its way backwards in time. We show a schematic overview of our adoption study paradigm in the electronic supplementary material, S6, figure E6.1)

Results

Discussion

An evolutionary model of sensitive periods when