1 Introduction
Understanding, quantifying, and predicting the ability of organisms to
adapt to changing environments is at the core of eco-evolutionary
research[1,2]. In the face of unprecedented environmental change,
natural populations, especially those with limited mobility, can avoid
extinction via phenotypic plasticity and/or adaptive
evolution [3]. However, our understanding of the interplay between
selection and plasticity in changing environments is surprisingly
limited[4–8]. This limitation is not trivial, for plasticity can
itself evolve[9], can be adaptive or nonadaptive[10], and has
seemingly contradictory effects on adaptive evolution[11], on which
we focus here. For decades, researchers have theorized whether
plasticity facilitates or hinders adaptive evolution[9,12]; the
evidence is contradictory and general patterns have not emerged
[5,10,11,13,14].
The primary conflicting hypotheses for whether plasticity facilitates or
hinders adaptive evolution are:
(H1) plasticity weakens directional selection by masking genotypic
variation (Bogert Effect [15]), thus slowing the rate of
genetic change[5,16–18] vs.
(H2) plasticity facilitates evolution by allowing the population to
persist under environmental change long enough for genetic change to
occur[19–22] (Plasticity-First Hypothesis [21] orBaldwin Effect [19]).
This debate remains unresolved, for even when theoretical predictions
agree with empirical findings[5,10,11,13,14,23], we lack a general
framework to ascertain the context-dependency of the prevalent
mechanism. Here, we introduce a framework based on environmental change
context, to outline clear null hypotheses for when and how plasticity
interacts with directional evolution. We place the plasticity
facilitates vs. hinders selection debate on two ends of a
continuum, and specify the properties of environmental
change–rate of mean change , variability , andtemporal autocorrelation –that influence how plasticity impacts
adaptive evolution.
The type of environmental change a population experiences can alter its
likelihood of adaptation and, ultimately, persistence[24–27].
Studies of demographic[28], genetic[29], and evolutionary
rescue[30], show that rate of mean change, variability, and temporal
autocorrelation of a population’s selective environment impact
population persistence[24,25,29,31–35]. However, because different
types of environmental change can have contradictory effects on
plasticity and evolution[34,36–38], elucidating these dynamics is
not trivial. Consequently, there is an urgent need to place this
discussion on the environmental stage in a generalizable way that will
allow ecologists and evolutionary biologists to better contextualize,
mechanistically understand, predict, and compare their findings.
Moving optimum theory links environmental change to the
resulting evolutionary responses. Three decades of research on this
theory shows that, when a population is confronted with an environment
that changes directionally, there is a critical rate of changethat must be matched by change in the mean phenotype of the population,
such that the mean remains close to the theoretical phenotypic
optimum . In this context, a phenotypic lag between the mean
phenotype and the optimum phenotype typically emerges which, if too
large, makes extinction certain [39–41]. Evolutionary (e.g. ,
selection, genetic variation) and ecological processes (e.g. ,
within-generation life history, plasticity and population dynamics)
together influence the limit of how far a population can lag without
going extinct. The contribution of plasticity to population persistence
and adaptation is largely determined by this phenotypic lag: how much of
the short- or long-term lag can be compensated for or even hindered by
plasticity?
We argue that hypotheses such as the Bogert Effect and the
Plasticity-First Hypothesis / Baldwin Effect are not mutually exclusive.
Rather, plasticity may facilitate or hinder adaptive evolution depending
on the properties of environmental change. To assess the impact of
plasticity on the ability of a population to evolutionarily track a
changing environmental optimum, we specify the links among the type of
environmental change, plasticity, and adaptive evolution by considering
several fundamental processes. Thus, we utilize both theoretical and
experimental studies to:
Assess how three key components of environmental change (rate of
mean change , variability , and temporal autocorrelation )
each alter the mechanisms behind phenotypic tracking of a moving
optimum ([i] Genetic variation, heritability, and
selection , and [ii] life history, plasticity andpopulation dynamics ).
Introduce a unified framework of testable hypotheses detailing how
those three components of environmental change can influence the
relative benefit of plasticity to adaptive evolution.