Abstract
Populations adapt to novel environmental conditions by genetic changes
or phenotypic plasticity. Plastic responses are generally faster and can
buffer fitness losses under variable conditions. Plasticity is typically
modelled as random noise and linear reaction norms that assume simple
one-to-one genotype-phenotype maps and no limits to the phenotypic
response. Most studies on plasticity have focused on its effect on
population viability. However, it is not clear, whether the advantage of
plasticity depends solely on environmental fluctuations or also on the
genetic and demographic properties (life histories) of populations. Here
we present an individual-based model and
study the relative importance of
adaptive and non-adaptive plasticity for populations of sexual species
with different life histories experiencing directional stochastic
climate change. Environmental fluctuations were simulated using
differentially autocorrelated climatic stochasticity or noise color, and
scenarios of directional climate change. Non-adaptive plasticity was
simulated as a random environmental effect on trait development, while
adaptive plasticity as a linear, logistic, or sinusoidal reaction norm.
The last two imposed limits to the plastic response and emphasized
flexible interactions of the genotype with the environment.
Interestingly, this assumption led to (i ) smaller phenotypic than
genotypic variance in the population and the coexistence of
polymorphisms, (ii ) many-to-one genotype-phenotype map, and
(iii ) the maintenance of higher genetic variation – compared to
linear reaction norms and genetic determinism – even when the
population was exposed to a constant environment for several
generations. Limits to plasticity led to genetic accommodation, when
costs were negligible, and to the appearance of cryptic variation when
limits were exceeded. We found that adaptive plasticity promoted
population persistence under red noise stochasticity and was
particularly important for life histories with low fecundity.
Populations producing more offspring could cope with environmental
fluctuations solely by genetic changes or random plasticity, unless
environmental change was too fast.
Keywords
Individual-based models; phenotypic plasticity; reaction norms; limits;
many-to-one genotype-phenotype map; developmental canalization;
evolvability; noise color; environmental change; stochastic fluctuations
Introduction
A prevailing challenge in ecology and evolutionary biology is to
understand and predict species’ responses to environmental change, such
as climate change (Chevin et al. 2010; Gonzalez et al. 2013).
Populations of different species are expected to respond to these
changes by adaptation to novel local environmental conditions, shifts in
their distributional range while tracking their preferred niche, or
local extinction (Franks et al. 2014; Wiens 2016). Particularly, when
movement opportunities are constrained, populations are expected to
either go extinct or to cope with novel conditions through adaptation by
genetic changes, or phenotypic plasticity. Phenotypic plasticity is
defined as the property of organisms sharing the same genotype to
produce different phenotypes, often in response to the local environment
(Pigliucci 2005; Reusch 2014; Sommer 2020). It constitutes the
non-heritable part of phenotypic variation and includes acclimation,
developmental plasticity, behavioral flexibility, learning, maternal
effects, epigenetics, and random noise (West-Eberhard 2003).
Among other factors, evolutionary rescue depends considerably on
demographic properties and the generation time of a species (Chevin et
al. 2010; Bell 2013). Thus, organisms that do not reproduce often or
produce relatively few progeny are expected to be vulnerable to
extinction under environmental change due to their lower supply of
beneficial mutations (Botero et al. 2015). Life history strategies where
a genetic response is limited, are expected to buffer fitness loss in a
novel environment through plastic responses, which are generally faster
(Lande 2009; Botero et al. 2015).Using individual-based models,
different life history strategies have been compared for their ability
to adapt to the local environment through genetic changes (e.g.,
Björklund et al. 2009). In contrast, the role of plasticity –
particularly, the role of different types of phenotypic plasticity –
for persistence under environmental change, has not yet been thoroughly
investigated relative to different life history strategies.
For
example, in species with similar generation time, those with relatively
high fecundity (“large clutch-size”) may rely less on plasticity as
compared to species with clutch-size limited to few offspring. Though it
was not the focus of their work, Björklund et al. (2009) observed in
their model that, all else equal, r-like life history strategists
persisted environmental change the longest (as compared to other life
history strategies) under scenarios of low heritability in which most
variability of the phenotypic trait was developed randomly (random
plasticity).
Phenotypic plasticity has long been considered important for organisms
experiencing fluctuating environmental conditions (Scheiner 1993; Via et
al. 1995). Yet, the modeling of phenotypic plasticity has not been a
straightforward task, since some features found in empirical research
remain elusive to current approaches (e.g., limits to plasticity, Murren
et al. 2015; many-to-one genotype-phenotype maps, Wagner 2005).
Models on the evolution of
phenotypic plasticity suggest that plasticity evolves in variable
environmental conditions, when cues are reliable and when costs are
relatively low (Ghalambor et al. 2007; Chevin et al. 2010; Reed et al.
2010; Lande 2014; Ashander et al. 2016; Ergon and Ergon 2016; Hendry
2016). However, year-to-year fluctuations of climatic variables such as
temperature can differ with regard to their serial autocorrelation
between consecutive time units (typically years; Laakso et al. 2001,
2004; Schwager et al. 2006; Björklund et al. 2009). How such
environmental stochasticity may promote the degree and mode of plastic
responses has received less attention. Ecological models have already
shown that environmental stochasticity reduces long-term population
growth and that the type (i.e., the color) of the stochastic noise
differently affects population extinction risk. For instance, Mustin et
al. (2013) found that extinction risk is expected to be high for
populations experiencing directional climate change and inhabiting
climates with reddish (i.e., positively autocorrelated) stochasticity.
However, they did not consider scenarios of negatively autocorrelated
stochastic noise (blue noise), nor the effect of plasticity on
population persistence.
Here,
we present an individual-based eco-evolutionary model to study the
relative importance of adaptive and non-adaptive plasticity for
populations of sexual species with different life histories,
experiencing scenarios of various rates of directional climate change
and different types of environmental stochasticity (noise color).
This paper deals with organisms
experiencing rapid environmental change and hence does not consider the
evolution of plasticity itself. Instead, it focuses on so far
understudied aspects of plasticity by (i ) specifically testing
for the influence of limits to plasticity, (ii ) exploring
developmental flexibility ; and (iii ) evaluating the performance
of different types of plasticity and life histories under environmental
change (e.g., we ask: what type of plasticity is preferred under a
particular life history?). Assuming limits to the plastic response may
add realism to the modeling of plasticity. For example, when costs of
plasticity are negligible, as it seems to be the case for the majority
of organisms (Murren et al. 2015), a model assuming perfect sensing and
no limits may arrive at perfectly adapted phenotypes under all
circumstances, while in nature, the plastic response is limited to a
definite range of environmental conditions, beyond which perfect
plasticity is physiologically impossible (Wiesenthal et al. 2018). This
is not the case, however, for linear reaction norms, where the perfect
plasticity is prevented only when assuming costs to plasticity or biased
perception of environmental cues. Most theoretical work in the
literature has focused on understanding the adaptive nature of
phenotypic plasticity (Via and Lande 1985; Nussey et al. 2007; Chevin et
al. 2010; Lande 2014), mainly using linear reaction norms and simple
one-to-one genotype-phenotype mapping (Chevin et al. 2010; Reed et al.
2010; Lande 2014). However, plasticity can result – at least for
quantitative traits – from a complex relationship between genotype and
phenotype, with the developmental system responding flexibly to internal
(genotype) and external inputs (environment) (Laland 2015). To this end,
we compare linear reaction norms with alternative plasticity types,
including a flexible developmental system. As a consequence, multiple
genotypes can have the same phenotype and are mutationally
interconnected (many-to-one genotype-phenotype map, Wagner 2008; Ahnert
2017; Aguilar-Rodríguez et al. 2018). This assumption leads to
interesting evolutionary and ecological outcomes that, to our knowledge,
are not captured by previous models, and that may be more in line with
what empirical evidence suggests.