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.