Sex-specific intergenerational plasticity I: maternal and paternal effects on sons and daughters

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 nonadaptive ways.

2. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of threespined 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, while 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, while predator-exposed mothers produced more anxious sons and daughters. Further, maternal and paternal effects on offspring survival were nonadditive: 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 nonadditive 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. 

Methods
Scototaxis and behavioral assay data were collected live and transcribed into Excel files. Opercular beat data and predation assay results were determined from video recordings.

1. 代际可塑性（intergenerational plasticity）或称亲本效应（parental effects），指亲本所处环境改变子代表型（phenotype）的现象，可影响生物体应对环境变化的能力。一个引人关注但尚未被充分探索的可能性是：亲本与子代的性别均能以适应性与非适应性两种方式，在代际可塑性的演化进程中发挥关键作用。
2. 本研究以三刺鱼（Gasterosteus aculeatus）的淡水种群为研究对象，通过独立与联合操控母本与父本的经历，分别评估二者对子代雌雄个体的表型效应，以此探究性别特异性亲本效应的存在潜力。我们验证了这一适应性假说：子代雌性对母本传递的信号更为敏感，而子代雄性则对父本传递的信号更为敏感。
3. 我们将母本、父本或双亲分别暴露于捕食风险的视觉信号环境中，并检测子代的抗捕食性状（antipredator traits）与脑组织基因表达（brain gene expression）水平。
4. 暴露于捕食风险的父本所产生的子代雄性表现出更高的风险倾向，而暴露于捕食风险的母本所产生的子代雌雄均表现出更强的焦虑水平。此外，亲本效应对子代存活的影响并非加性效应：仅父本经历捕食风险暴露（而非双亲均暴露）的子代，在面对活体捕食者时的存活率更低。脑组织基因表达同样存在显著的性别特异性效应：母本与父本暴露于捕食风险，会分别激活子代不同的转录谱（transcriptional profiles）；且子代雌雄在亲本经历对其脑组织基因表达谱的影响模式上存在显著差异。
5. 本研究未发现足够证据支持“子代优先响应同性亲本经历”这一假说。亲本效应会随亲本与子代的性别呈现复杂且非加性的变化模式。若忽略这类性别特异性模式（例如将雌雄子代合并分析），则会低估亲本效应的作用强度。综上，本研究结果凸显了性别对代际可塑性模式的潜在影响，并为代际可塑性与性别特异性选择压力、性冲突及性选择之间的交互关系提出了新的研究问题。

### 方法
趋暗行为（scototaxis）与行为检测数据通过活体采集后录入Excel文件。鳃盖运动（opercular beat）数据与捕食检测实验结果均通过视频录像分析获得。