Transgenerational plasticity of inducible defences: Combined effects of grand‐parental, parental and current environments

Abstract

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.

Transgenerational Plasticity in the Context of Predator-Prey Interactions

“…Agrawal et al (1999) showed that the morphological defense of D. cucullata (relative helmet length) induced in F1 offspring from F0 predator-exposed parents disappeared in F2 offspring (pattern 1 in Figure 3). A similar pattern was found for clutch size in D. ambigua (Walsh et al, 2015), total length and stress-induced cortisol in the three-spined stickleback G. aculeatus (Hellmann et al, 2020), and for body mass and shell size in the freshwater snail P. acuta (Tariel et al, 2020): in all cases, the transgenerational effect disappeared in the F2 generation (no effect of the grand-parental environment). In contrast, Yin et al (2015) demonstrated grand-maternal induction of defensive morphology (posterolateral spine) in rotifers B. calyciflorus.…”

“…In contrast, Yin et al (2015) demonstrated grand-maternal induction of defensive morphology (posterolateral spine) in rotifers B. calyciflorus. Similarly, Tariel et al (2020) found that grand-parental exposure to predator-cues influenced escape behavior and shell thickness in P. acuta. For age at maturation in D. ambigua, predator-induced TGP (earlier maturation) was detectable two generations following cue removal (i.e., until the F2 generation), and finally disappeared in the F3 (Walsh et al, 2015).…”

“…For age at maturation in D. ambigua, predator-induced TGP (earlier maturation) was detectable two generations following cue removal (i.e., until the F2 generation), and finally disappeared in the F3 (Walsh et al, 2015). Interestingly, the transgenerational effect in the F2 generation was lower than in the F1 in all studies (Walsh et al, 2015;Yin et al, 2015;Tariel et al, 2020), indicating a decline of transgenerational response to predation over time (pattern 3 in Figure 3). Moreover, Hellmann et al (2020) observed in G. aculeatus that predator-induced TGP persisted in a lineagespecific (through the grand-maternal or grand-paternal lineage) and in a sex-specific (only in male or female grand-offspring) way: F2 females were heavier and had a reduced anti-predator response (reduced activity after a simulated predator attack) when their paternal grandfather was exposed to predator-cues, while F2 males had a reduced anti-predator response (frozen and escape behavior) when their maternal grandfather was exposed to predator-cues.…”

“…Most of the studies reviewed here (87%) investigated predatorinduced TGP over two generations only (F0 and F1). In the following, we summarize the results of seven studies that explored the influence of past exposure to predation over three (Agrawal et al, 1999;Yin et al, 2015;Hales et al, 2017;Hellmann et al, 2020;Tariel et al, 2020), four (Walsh et al, 2015) or five generations (Sentis et al, 2018). Agrawal et al (1999) showed that the morphological defense of D. cucullata (relative helmet length) induced in F1 offspring from F0 predator-exposed parents disappeared in F2 offspring (pattern 1 in Figure 3).…”

Interactions Between Maternal, Paternal, Developmental, and Immediate Environmental Effects on Anti-predator Behavior of the Snail Physa acuta

“…In this laboratory study, we investigated how effects of maternal, paternal and personal (both developmental and immediate) exposures to cues of predator presence interact to shape anti-predator behaviors. Many prey engage in antipredatory behaviors when they or their parents detect predator cues (predator-induced WGP: Lima and Dill, 1990; predatorinduced TGP: review in Tariel et al, 2020). We used the freshwater snail Physa acuta as our model system.…”