Empirical patterns of environmental variation favor adaptive transgenerational plasticity.

Jack M Colicchio,Jacob Herman

doi:10.1002/ece3.6022

Abstract

Effects of parental environment on offspring traits have been well known for decades. Interest in this transgenerational form of phenotypic plasticity has recently surged due to advances in our understanding of its mechanistic basis. Theoretical research has simultaneously advanced by predicting the environmental conditions that should favor the adaptive evolution of transgenerational plasticity. Yet whether such conditions actually exist in nature remains largely unexplored. Here, using long‐term climate data, we modeled optimal levels of transgenerational plasticity for an organism with a one‐year life cycle at a spatial resolution of 4 km2 across the continental United States. Both annual temperature and precipitation levels were often autocorrelated, but the strength and direction of these autocorrelations varied considerably even among nearby sites. When present, such environmental autocorrelations render offspring environments statistically predictable based on the parental environment, a key condition for the adaptive evolution of transgenerational plasticity. Results of our optimality models were consistent with this prediction: High levels of transgenerational plasticity were favored at sites with strong environmental autocorrelations, and little‐to‐no transgenerational plasticity was favored at sites with weak or nonexistent autocorrelations. These results are among the first to show that natural patterns of environmental variation favor the evolution of adaptive transgenerational plasticity. Furthermore, these findings suggest that transgenerational plasticity is likely variable in nature, depending on site‐specific patterns of environmental variation.

Highlights

Natural selection can produce adaptation only if the selective environment is reliably encountered over generations, or in other words, if selective environments are statistically predictable
A critical question has remained unanswered: do natural patterns of environmental variation contain fluctuations of intermediate environmental grain that favor the evolution of adaptive transgenerational plasticity? Our analysis of years of climatic data from the continental U.S revealed that such patterns are widespread
We demonstrate that patterns of climatic variation in nature may favor the adaptive evolution of transgenerational plasticity in organisms with approximately annual generation times, such as annual plants

Summary

Introduction

Natural selection can produce adaptation only if the selective environment is reliably encountered over generations, or in other words, if selective environments are statistically predictable. Models of evolution envisioned fitness landscapes that were static, such that populations adapt over the course of generations to one or another environment (Fisher 1930). While this form of adaptation optimizes phenotypes in homogenous environments, the more realistic scenario of environmental heterogeneity in both space and time limits the adaptive value of such constitutive genetic expression Over the last three decades, it has become clear that effects of parental environments on offspring phenotypes (i.e., transgenerational plasticity) are remarkably common (reviewed by (Mousseau and Fox 1998; Uller 2008; Bonduriansky and Day 2009; Holeski et al 2012; Conrath et al 2015; Sultan 2015). When Mimulus guttatus plants experience herbivory, their offspring increase production of defensive leaf trichomes (Holeski 2007; Colicchio et al 2015; Colicchio 2017)

Methods

Results

Discussion

Conclusion