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

Abstract

Transgenerational plasticity, which occurs when the environment experienced by parents changes the phenotype of offspring, is widespread in animal and plant species. Both maternal and paternal environments can underlie transgenerational plasticity, but experimental studies unraveling how their effects interact together and with the personal (both developmental and immediate) environments are still rare. Yet unraveling these interactions is fundamental to understanding how offspring integrate past and present environmental cues to produce adaptive phenotype. Using the hermaphroditic and freshwater snail Physa acuta, we tested how predator cues experienced by offspring, mothers and fathers interact to shape offspring anti-predator behavior. We raised a first generation of snails in the laboratory with or without chemical predator cues and realized full-factorial crosses to disentangle maternal and paternal cues. We then raised the second generation of snails with or without predator cues and assessed, when adults, their escape behavior in two immediate environments (with or without predator cues) and activity in the immediate environment without predator cues. We found that personal, maternal, and paternal predator cues interacted to shape offspring escape behavior and activity. Firstly, for escape behavior, snails integrated the cues from developmental and parental environments only when exposed to predator cues in their immediate environment, suggesting that personal immediate experience must corroborate the risky parental environment to reveal transgenerational plasticity. For activity, this same hypothesis helps explain why no clear pattern of transgenerational plasticity was revealed, as activity was only measured without predator cues in the immediate environment. Secondly, a single maternal exposure to predator cues decreased offspring escape behavior while a single paternal exposure had no effect, surprisingly demonstrating sex-specific transgenerational plasticity for a simultaneous hermaphroditic species. Thirdly, when both mother and father were exposed, paternal cues were integrated by offspring according to their own developmental environment. The paternal exposure then mitigated the reduction in escape behavior due to the maternal exposure only when offspring developed in control condition. Overall, our study highlighted complex patterns of sex-specific transgenerational plasticity resulting from non-additive interactions between parental, developmental and immediate experiences.

Paternal care effects outweigh gamete-mediated and personal environment effects during the transgenerational estimation of risk in fathead minnows

“…The only significant effect of high personal risk emerged following the stimulus (Fig. 3 a), matching the finding that some level of immediate risk is required to reveal the effects of background risk exposure [ 48 , 75 ]. High personal risk appears to reduce risk allocation to a greater extent the less information about high-risk is present in the parental generation, culminating in a significantly reduced risk allocation only when both parents were derived from a low-risk environment (Fig.…”

“…2 a and 3 a), suggesting the presence of sex-specific transgenerational plasticity [ 21 ]. The general direction of paternal effects mostly outweighing maternal effects contrasts other studies across taxa suggesting that usually maternal effects outweigh paternal effects [snails: 75 , birds: 76 , fish: 77 ]. Our observation is still in accordance with many studies highlighting the relevance of paternal effects [ 78 , 79 ], and a recent meta-analysis suggesting that paternal effect sizes are on average larger than maternal ones [ 61 ].…”

No effects of waterproof marking on the behaviour and growth of Physa acuta Draparnaud, 1805 (Gastropoda: Hygrophila: Physidae) in the laboratory

“…The absence of marking effects on snail activity in our experiment with P. acuta is compatible with earlier findings of absence of marking effects on snail activity, locomotion, horizontal dispersion, anti-predator behaviour, reproductive behaviour, susceptibili-ty to parasite infection, and survival for P. acuta and other aquatic gastropod species (FEnwick & amin 1983, o'keeFFe 1985, Goater et al 1989, burris et al 1990, mcraE & lEPitzki 1994, henry & Jarne 2007, häderer et al 2009, coutEllEc & caquEt 2011, morton & silliman 2020, tariel et al 2020.…”

“…Although marking individual animals for observational/experimental purposes is a common practice (heidinGer et al 2009 and references therein), it has seldom been used for gastropods (henry & Jarne 2007). The few studies that used individual markings on terrestrial or aquatic gastropods did not show any negative marking effects on snails (FEnwick & amin 1983, o'keeFFe 1985, baker 1988, burris et al 1990, Gosselin 1993, mcraE & lEPitzki 1994, baminGer 2000, henry & JarnE 2007, tariel et al 2020. The most common ways to mark individual snails were plastic tags attached with some kind of glue, nail varnish, enamel, or waterproof car-body paint (review in henry & Jarne 2007).…”

Beyond compliance: harmonising research and husbandry practices to improve experimental reproducibility using fish models

“…By contrast, behavioural neuroscientists and those studying epigenetics have a heightened need to understand the life experience of their study animals as this can (and often does) impact the outcome of their research. For example, the environment that animals experience during early life has been shown to affect subsequent rates of development (Eyck et al ., 2019), behavioural responses (Carlson, 2017), brain structure and function (Eachus, Choi & Ryu, 2021) and to have trans‐generational effects in the offspring (Tariel, Luquet & Plenet, 2020). For example, female three‐spined sticklebacks exposed to predators as a stressful encounter have been shown to produce larger eggs than non‐exposed females and their offspring show increased anti‐predator behaviour (Giesing et al ., 2011).…”