Transgenerational plasticity of exploratory behavior and a hidden cost of mismatched risk environments between parental sexes

Abstract

We require a better understanding of the relative contribution of different modes of non-genetic inheritance in behavioral trait development. Thus, we investigate variation in exploratory behavior, which is ecologically relevant and a target of selection. The metabolic hypothesis predicts exploratory behavior to be size-dependent across taxa. This size-dependency is cancelled out under high perceived risk, allowing us to determine the transgenerationally integrated estimated level of risk. Using fathead minnows Pimephales promelas, we manipulated perceived risk in mothers, fathers, caring males and offspring through continuous exposure to either conspecific alarm cues or to a control water treatment. In 1000 four-month old offspring, we determined body sizes and exploratory behavior. Perceived high risk in mothers, followed by personal risk, was most effective in eliminating size-dependent behavior whereas effects of paternal risk on offspring behavioral development were substantially weaker. When maternal risk is high, environmental mismatches between parents prevented offspring from responding appropriately to personal high risk. The environment of the caring male also impacted offspring behavior to a greater extent than that of its genetic parents. Our study highlights the high relative importance of maternal, personal and caring male risk environments and showcases potential costs of an environmental mismatch between parental sexes.

Neglected patterns of variation in transgenerational plasticity: The importance of different sources of environmental variation differs across ages and sexes in a cyprinid fish

“…Our first observation that maternal environmental experience consistently outweighed personal environmental experience across ontogeny and sexes is in accordance with previous research on earlier developmental stages of the same species (Meuthen et al, 2021(Meuthen et al, , 2023 and with a meta-analysis suggesting the same to be true for maternal effects in behaviour and physiology across taxa (Moore et al, 2019). At the same time, this result appears to be in opposition to the "sampling-duration" theory.…”

“…Third, both gamete-mediated and care-mediated environmental experience were equally important for the formation of morphological defences in juveniles, in accordance with previous P. promelas research (Meuthen et al, 2021(Meuthen et al, , 2023. In adult males, gamete-mediated information emerged to be more relevant instead, which is in accordance with Hellmann et al (2021), and supports to our "gametic-care-ontogenetic-switch" hypothesis.…”

“…Because predator preferences are driven by relative differences between prey items (Stige et al, 2019), even small phenotypic changes can still contribute to enhanced survival. Moreover, cue-induced TGP manifests not only in P. promelas morphology but also in behaviour (Meuthen et al, 2021(Meuthen et al, , 2023.…”

“…Here, we comprehensively study these four theories by taking advantage of cue-induced antipredator defences, which are one of the first described cases of adaptive phenotypic plasticity (Brönmark & Miner, 1992) and one of the most convincing examples of adaptive TGP (Uller et al, 2013). As our model system, we use the fathead minnow Pimephales promelas, an established model system for antipredator TGP (Crane et al, 2021;Meuthen et al, 2021Meuthen et al, , 2023. This small (6.0-7.4 cm) sexually dimorphic common prey cyprinid fish is widespread across Northern American freshwaters (Scott & Crossman, 1998).…”