When to rely on maternal effects and when on phenotypic plasticity?

Abstract

Existing insight suggests that maternal effects have a substantial impact on evolution, yet these predictions assume that maternal effects themselves are evolutionarily constant. Hence, it is poorly understood how natural selection shapes maternal effects in different ecological circumstances. To overcome this, the current study derives an evolutionary model of maternal effects in a quantitative genetics context. In constant environments, we show that maternal effects evolve to slight negative values that result in a reduction of the phenotypic variance (canalization). By contrast, in populations experiencing abrupt change, maternal effects transiently evolve to positive values for many generations, facilitating the transmission of beneficial maternal phenotypes to offspring. In periodically fluctuating environments, maternal effects evolve according to the autocorrelation between maternal and offspring environments, favoring positive maternal effects when change is slow, and negative maternal effects when change is rapid. Generally, the strongest maternal effects occur for traits that experience very strong selection and for which plasticity is severely constrained. By contrast, for traits experiencing weak selection, phenotypic plasticity enhances the evolutionary scope of maternal effects, although maternal effects attain much smaller values throughout. As weak selection is common, finding substantial maternal influences on offspring phenotypes may be more challenging than anticipated.

Local adaptation in transgenerational responses to predators

“…Exposure to predator cues during generation 1 facilitated stronger withingeneration responses in Daphnia from lakes with anadromous alewife as these populations matured earlier than Daphnia from landlocked and no alewife lakes (figure 2; see also [35,36,[40][41][42]). Consistent with recent theory suggesting that the evolution of within-versus among-generation plasticity can be decoupled [25][26][27], we observed the opposite responses across generations. Daphnia from landlocked and no alewife lakes strongly programmed offspring for faster development in the second experimental generation, whereas these transgenerational responses were weak in Daphnia from lakes with anadromous alewife (figures 2 and 4).…”

“…Strong seasonal pulses in predation are associated with the evolution of withingeneration plasticity [35], whereas low temporal variability in predator-induced mortality is correlated with increased TGP (see conceptual figure electronic supplementary material, figure S3). Recent theory [25][26][27] identified environmental stability as one of the key determinants of selection on transgenerational inheritance, with high temporal stability favouring the evolution of increased TGP. This is because TGP decreases the likelihood of environmentally mismatched phenotypes (between parent and offspring) when the rate of environmental change is low compared with generation time.…”

“…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.…”

“…That is, within-and across-generation responses will respond in a similar fashion to environmental signals to improve fitness. Only recently, however, has theory identified the ecological selective pressures that may act independently on within-and across-generation responses [25][26][27]. In particular, within-generation plasticity is favoured when there exists high temporal variability in the environment, whereas low temporal variability and a slow rate of environmental change are predicted to favour across-generation responses (figure 1) [25].…”

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

“…Recent theoretical models and meta‐analysis have been generated to examine the evolution of parental and maternal effects generally (e.g., Kuijper & Hoyle, 2015; Leimar & McNamara, 2015; Uller, Nakagawa, & English, 2013). Using insights from these theoretical models in addition to those from error management theory (EMT; Haselton & Buss, 2000), we provide a framework for generating field‐testable hypotheses regarding the adaptive potential of maternal stress under different scenarios.…”