1. Intergenerational plasticity or parental effects-when parental environments alter the phenotype of future generations-can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex-of both the parent and the offspring-plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. 2. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. 3. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. 4. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. 5. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.
words) 16Sex-specific selection pressures can generate different phenotypic optima for males and 17 females in response to the current environment, i.e. sex differences in phenotypic plasticity. Less 18 widely appreciated is the possibility that transgenerational plasticity (TGP) can also depend on 19 sex. Sex-specific TGP is potentially of great evolutionary significance, as it is a mechanism by 20 which mothers and fathers can exert different effects on offspring traits and by which potentially 21 adaptive traits can persist selectively across generations via only daughters or sons. Here, we 22 demonstrate that maternally-and paternally-mediated TGP in response to predation risk have 23 largely distinct effects on offspring traits in threespined sticklebacks (Gasterosteus aculeatus). 24 Predator-exposed fathers produced sons that were more risk-prone, while predator-exposed 25 mothers produced more anxious sons and daughters. Further, when combined together, maternal 26 and paternal environments on offspring survival were nonadditive. Such sex-specific effects 27 could occur if predation risk causes mothers and fathers to activate different developmental 28 programs in sons versus daughters. Consistent with this hypothesis, offspring brain gene 29 expression profile depended on whether their mother and/or father had been exposed to risk, and 30 the influence of maternal and paternal environments varied between male and female offspring. 31Altogether these results draw attention to the potential for sex to influence patterns of TGP, and 32 raise new questions about the evolution of plasticity at the interface between sexual conflict and 33 parent-offspring conflict, with paternal strategies, maternal strategies, and offspring counter-34 adaptations all ultimately dictating offspring phenotypes. 35 36 Key words: maternal effect, paternal effect, Gasterosteus aculeatus, phenotypic plasticity, 37 intergenerational plasticity, nongenetic inheritance 38Significance 39 TGP helps organisms cope with environmental change by bridging the gap between 40 within-generational plasticity and long-term evolutionary change. Sex-specific TGP may allow 41 mothers and fathers to selectively alter the phenotypes of their sons and daughters in response to 42 the environment with a greater degree of precision than genetic inheritance and in ways that 43 match the distinct life-history strategies of males and females. By isolating cues coming from 44 mothers versus fathers and separately evaluating phenotypic effects in sons versus daughters, we 45show that interactions between maternal cues, paternal cues, and offspring sex are integral to 46 understanding when and how the past environment influences future phenotypes, and the 47
Parental effects can help offspring cope with challenging environments, but whether these effects are unique to specific environmental conditions is largely unknown. Parental effects may evolve via a core pathway that generally prepares offspring for risky environments or could be stimuli-specific, with offspring developing phenotypes that are tailored to specific environmental challenges. We exposed threespined sticklebacks (Gasterosteus aculeatus) fathers to a potentially threatening stimulus (net) versus native predator (sculpin). Offspring of sculpin-exposed fathers were more responsive (greater change in activity) to a simulated predator attack, while offspring of net-exposed fathers were less responsive (lower plasma cortisol and fewer antipredator behaviors). To evaluate offspring response to native and non-native stimuli, we sequentially exposed offspring of netexposed, sculpin-exposed or control fathers to a net, native sculpin model, or non-native trout model. Paternal treatment did not influence offspring response to stimuli; instead, offspring were more responsive to the native sculpin predator compared to nets or non-native trout predator. Collectively, we demonstrate that sperm-mediated paternal effects in response to different, potentially stressful stimuli result in distinct offspring phenotypes. This specificity may be key to understanding the evolution of adaptive parental effects and how parents prime offspring for encountering both evolved and novel environmental stimuli.
15Parental effects can help offspring cope with challenging environments, but whether 16 these effects are unique to specific environmental conditions is largely unknown. Parental 17 effects may evolve via a core pathway that generally prepares offspring for risky 18 environments or could be stimuli-specific, with offspring developing phenotypes that are 19 tailored to specific environmental challenges. We exposed threespined sticklebacks 20 (Gasterosteus aculeatus) fathers to a potentially threatening stimulus (net) versus native 21 predator (sculpin). Offspring of sculpin-exposed fathers were more responsive (greater 22 change in activity) to a simulated predator attack, while offspring of net-exposed fathers were 23 less responsive (lower plasma cortisol and fewer antipredator behaviors). To evaluate 24 offspring response to native and non-native stimuli, we sequentially exposed offspring of net-25 exposed, sculpin-exposed or control fathers to a net, native sculpin model, or non-native trout 26 model. Paternal treatment did not influence offspring response to stimuli; instead, offspring 27 were more responsive to the native sculpin predator compared to nets or non-native trout 28 predator. Collectively, we demonstrate that sperm-mediated paternal effects in response to 29 different, potentially stressful stimuli result in distinct offspring phenotypes. This specificity 30 may be key to understanding the evolution of adaptive parental effects and how parents prime 31 offspring for encountering both evolved and novel environmental stimuli. 32 33 34
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