Transitions in paternal social status predict patterns of offspring growth and metabolic transcription

Parental effects occur when changes in the parental phenotype or environment cause changes to offspring phenotype. While some parental effects are triggered in response to an environmental cue in a time-locked fashion, other parental effects persist even after the cue has been removed, suggesting multiple timescales of action. For parental effects to serve as reliable signals of current environmental conditions, they should be reversible, such that when the cue changes, offspring phenotypes change in accordance. Social hierarchy is a prevalent feature of the environment, and current parental social status could signal the environment in which offspring will be born. Here, we sought to address parental effects of social status and their timescale of action in mice. We show that competition in seminatural environments affects offspring growth rate. Although dominant males are not heavier than nondominant or control males, they produce faster growing offspring, particularly sons. The timing, effect-size, and sex-specificity of this association are modulated by maternal social experience. We show that a change in paternal social status is sufficient to modulate offspring weight: from one breeding cycle to the next, status-ascending males produce heavier sons than before, and status-descending males produce lighter sons than before. Current paternal status is also highly predictive of liver transcription in sons, including molecular pathways controlling oxidative phosphorylation and iron metabolism. These results are consistent with a parental effect of social experience, although alternative explanations are considered. In summary, changes in paternal social status are associated with changes in offspring growth and metabolism.

亲代效应（parental effects）指当亲代表型或所处环境发生改变时，可引发后代表型产生相应变化的生物学现象。部分亲代效应会以时间锁定的方式响应环境线索而触发，而另一些亲代效应则会在环境线索移除后仍持续存在，这提示其作用存在多种时间尺度。
若要使亲代效应成为当前环境条件的可靠信号，其应当具备可逆性——即当环境线索发生改变时，后代表型也会随之同步调整。社会层级是一类广泛存在的环境特征，亲代当前的社会地位可作为子代即将所处环境的信号。
本研究旨在探究小鼠体内由社会地位介导的亲代效应及其作用时间尺度。我们发现，半自然环境中的竞争会对子代生长速率产生影响。尽管优势雄性小鼠的体重并未显著高于非优势或对照组雄性，但其子代的生长速度更快，尤以雄性子代最为明显。该关联的发生时序、效应大小以及性别特异性，均会受到母方社会经历的调控。
我们证实，父代社会地位的改变足以调控子代体重：在不同繁殖周期之间，社会地位上升的雄性小鼠所产的雄性子代体重较此前更高，而社会地位下降的雄性小鼠所产的雄性子代体重则较此前更低。当前父代的社会地位还可高度预测雄性子代的肝脏转录特征，其中包含调控氧化磷酸化与铁代谢的分子通路。
上述结果与社会经历介导的亲代效应相符，同时本研究也对其他替代性解释进行了探讨。总而言之，父代社会地位的改变与子代生长及代谢的变化存在显著关联。