Abstract

Parental effects may help offspring respond to challenging environments, but whether parental exposure to different environmental challenges induces similar responses in offspring is largely unknown. We compared the offspring of threespine stickleback (Gasterosteus aculeatus) fathers who had been exposed to a potentially threatening stimulus (net), a native predator (sculpin), or who had been left unexposed (control). Relative to offspring of control fathers, offspring of sculpin-exposed fathers were more responsive (greater change in activity) to a simulated sculpin predator attack, while offspring of net-exposed fathers were less responsive (fewer antipredator behaviors) and showed altered stress responses compared to the control. To evaluate whether parental exposure primes offspring to respond to specific stimuli (e.g., offspring of net-exposed fathers respond most strongly to a net), we then exposed offspring of each paternal treatment to nets, native sculpin models, or non-native trout models. Paternal treatment did not influence offspring response to different stimuli; instead, offspring were generally more responsive to the native sculpin predator compared to nets or non-native trout predator, suggesting that sticklebacks have innate predator recognition of native predators. Collectively, these results underscore that, while parental exposure to non-ecologically relevant stressors elicits effects in intergenerational studies, these findings may not mirror those produced when parents encounter ecologically relevant stressors. Knowing that parental effects can be predator-specific furthers our understanding of the ways in which parental effects may evolve to be adaptive and suggests the potential for transgenerational plasticity to affect how animals respond to human induced environmental change, including non-native predators.

Significance statement

Despite extensive evidence for parental effects, we have very little knowledge regarding whether parental effects are stimuli-specific. Here, we found that paternal exposure to different, potentially stressful stimuli prior to fertilization has specific effects on offspring traits: paternal exposure to a model of a sculpin (a native predator) heightened offspring responsivity to simulated predation risk, while paternal exposure to an artificial stimulus/stressor (net) reduced offspring antipredator behavior relative to the control. We found no evidence that offspring responded more strongly to the stimulus that their father encountered; instead, offspring were overall more responsive to a sculpin predator compared to a net or non-native trout. Overall, these results suggest that sperm-mediated paternal effects can be highly specific, and while non-ecologically relevant stimuli elicit effects in intergenerational studies, these effects may differ from those that occur when parents are exposed to native, ecologically relevant stimuli.

中文翻译：

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三刺棘鱼精子介导的父系效应的特异性

摘要

父母的影响可能有助于后代对具有挑战性的环境做出反应，但父母暴露于不同的环境挑战是否会在后代中引起类似的反应在很大程度上是未知的。我们比较了刺棘鱼 ( Gasterosteus aculeatus)的后代) 暴露于潜在威胁性刺激（净）、本地捕食者（杜鹃）或未暴露（对照）的父亲。相对于对照组父亲的后代，暴露于杜鹃鱼父亲的后代对模拟的杜鹃捕食者攻击反应更灵敏（活动变化更大），而暴露于网络的父亲的后代反应较弱（较少的反捕食者行为）并且显示出应激反应改变到控件。为了评估父母的暴露是否会引发后代对特定刺激的反应（例如，暴露于网络的父亲的后代对网络的反应最强烈），然后我们将每种父亲处理的后代暴露于网络、本地杜鹃模型或非本地鳟鱼模型. 父亲的待遇不影响后代对不同刺激的反应；反而，与网或非本地鳟鱼捕食者相比，后代通常对本地杜鹃捕食者更敏感，这表明棘鱼对本地捕食者具有天生的捕食者识别能力。总的来说，这些结果强调，虽然父母暴露于非生态相关压力源会在代际研究中产生影响，但这些发现可能无法反映父母遇到生态相关压力源时产生的结果。了解亲代效应可能是特定于捕食者的，这进一步加深了我们对亲代效应可能进化为适应性方式的理解，并表明跨代可塑性可能会影响动物对人类引起的环境变化（包括非本地捕食者）的反应。这表明棘鱼对本地捕食者具有天生的捕食者识别能力。总的来说，这些结果强调，虽然父母暴露于非生态相关压力源会在代际研究中产生影响，但这些发现可能无法反映父母遇到生态相关压力源时产生的结果。了解亲代效应可能是特定于捕食者的，这进一步加深了我们对亲代效应可能进化为适应性方式的理解，并表明跨代可塑性可能会影响动物对人类引起的环境变化（包括非本地捕食者）的反应。这表明棘鱼对本地捕食者具有天生的捕食者识别能力。总的来说，这些结果强调，虽然父母暴露于非生态相关压力源会在代际研究中产生影响，但这些发现可能无法反映父母遇到生态相关压力源时产生的结果。了解亲代效应可能是特定于捕食者的，这进一步加深了我们对亲代效应可能进化为适应性方式的理解，并表明跨代可塑性可能会影响动物对人类引起的环境变化（包括非本地捕食者）的反应。虽然父母暴露于非生态相关压力源会在代际研究中产生影响，但这些发现可能无法反映父母遇到生态相关压力源时产生的结果。了解亲代效应可能是特定于捕食者的，这进一步加深了我们对亲代效应可能进化为适应性方式的理解，并表明跨代可塑性可能会影响动物对人类引起的环境变化（包括非本地捕食者）的反应。虽然父母暴露于非生态相关压力源会在代际研究中产生影响，但这些发现可能无法反映父母遇到生态相关压力源时产生的结果。了解亲代效应可能是特定于捕食者的，这进一步加深了我们对亲代效应可能进化为适应性方式的理解，并表明跨代可塑性可能会影响动物对人类引起的环境变化（包括非本地捕食者）的反应。

意义声明

尽管有大量关于亲代效应的证据，但我们对亲代效应是否具有刺激特异性知之甚少。在这里，我们发现父亲在受精前暴露于不同的、潜在的压力刺激对后代的特征有特定的影响：父亲暴露于杜鹃模型（本地捕食者）提高了后代对模拟捕食风险的反应，而父亲暴露于人工相对于对照，刺激/应激源（净）减少了后代的反捕食者行为。我们没有发现后代对父亲遇到的刺激反应更强烈的证据；相反，与网状或非本地鳟鱼相比，后代总体上对杜鹃捕食者反应更灵敏。总体而言，这些结果表明精子介导的父系效应具有高度特异性，