The fitness costs of adaptation via phenotypic plasticity and maternal effects

Abstract

Summary1. Phenotypes are often environmentally dependent, which requires organisms to track environmental change. The challenge for organisms is to construct phenotypes using the most accurate environmental cue. 2. Here, we use a quantitative genetic model of adaptation by additive genetic variance, within-and transgenerational plasticity via linear reaction norms and indirect genetic effects respectively. 3. We show how the relative influence on the eventual phenotype of these components depends on the predictability of environmental change (fast or slow, sinusoidal or stochastic) and the developmental lag s between when the environment is perceived and when selection acts. 4. We then decompose expected mean fitness into three components (variance load, adaptation and fluctuation load) to study the fitness costs of within-and transgenerational plasticity. A strongly negative maternal effect coefficient m minimizes the variance load, but a strongly positive m minimises the fluctuation load. The adaptation term is maximized closer to zero, with positive or negative m preferred under different environmental scenarios. 5. Phenotypic plasticity is higher when s is shorter and when the environment changes frequently between seasonal extremes. Expected mean population fitness is highest away from highest observed levels of phenotypic plasticity. 6. Within-and transgenerational plasticity act in concert to deliver well-adapted phenotypes, which emphasizes the need to study both simultaneously when investigating phenotypic evolution.

Local adaptation in transgenerational responses to predators

“…For these populations, exposure to a predator cue essentially forecasts the presence of a predator for the immediate future. The observed within-generation response in this population aligns then with theoretical expectations for organisms inhabiting seasonal environments [22][23][24][25][26][27]. Given that the presence of a predator varies in these lakes, parental Daphnia are not expected to adaptively alter the phenotypes of future generations.…”

“…The extent to which the observed delay size at maturation (mm) in development rate across generations is maladaptive or simply reflects trade-offs associated with responses within and across generations is unclear ( [15] and see also [44]). It is also important to note that the induction of TGP in a temporally varying environment depends upon the rate of environmental change in relation to the generation length of the organism [22][23][24][25][26][27]. TGP is expected to evolve when the environment changes infrequently compared with the generation length of the organism.…”

Predator-induced phenotypic plasticity within- and across-generations: a challenge for theory?

“…Transgenerational responses are expected to be favoured when there is environmental heterogeneity across generations and when offspring environmental conditions are predictable from parental environmental conditions [2,3,[20][21][22]. Current theory that explicitly incorporates phenotypic plasticity and 'maternal effects' [23,24] indicates that predictable environmental variation will simultaneously select for increased plasticity within-and across-generations. However, the covariation between within-and across-generation plasticities has not yet received any empirical evaluation.…”

Maternal Effects in a Wild Songbird Are Environmentally Plastic but Only Marginally Alter the Rate of Adaptation

“…Had we included a realistic adult survival rate (for great tits circa 0.5) in the model, the effect of the maternal effect on the evolutionary response would have been even more reduced due to increased generation time, indicating even more strongly that the evolutionary consequences of the maternal effect on clutch size in our population are negligible. Indeed, had we used extreme parameter values used in theoretical model exercises (e.g., Hoyle and Ezard 2012;Ezard et al 2014;Prizak et al 2014), the effects would have been more profound ( fig. S5).…”

“…Different scenarios can then be explored, varying m and predicting its role in adaptation and fitness in combination with other adaptive mechanisms such as phenotypic plasticity and grand-maternal effects (Hoyle and Ezard 2012;Ezard et al 2014;Prizak et al 2014). In reality, however, maternal effects may not be fixed but plastic in response to environmental conditions and hence may change from season to season.…”