Maternal social environment shapes yolk testosterone allocation and embryonic neural gene expression in tree swallows

A female's behavioral and physiological response to her environment can have lasting effects on the development of her offspring. This type of non-genetic inheritance (or maternal effect) occurs across taxa but is particularly well-studied in birds due to the relative ease of measuring maternal hormones in externally developing eggs. For example, females breeding in areas of high social competition allocate more of the hormone testosterone (T) to their egg yolks. These high-T offspring exhibit numerous phenotypic changes, including faster juvenile growth and enhanced aggression well into adulthood, which are potentially beneficial traits in high-competition areas. Thus, females may be able to communicate the current social environment to their offspring and prepare them for adverse conditions. Yet, the proximate mechanisms underlying how maternal hormones affect offspring are largely ignored, impairing our understanding of an ecologically important source of phenotypic plasticity. Here, we explored the effects of the maternal social environment on yolk T allocation and genome-wide patterns of neural gene expression in male and female tree swallow (Tachycineta bicolor) embryos. We observed a population of free-living tree swallows breeding at sites with variable breeding densities. We performed behavioral observations to record the rate of physical aggression at these sites, which was significantly higher at high density sites. We collected eggs at two developmental timepoints: the day laid to measure maternally derived T concentrations and embryonic day 11 (ED11) to measure gene expression patterns in whole brains using RNA-seq. We took a genome-wide approach to help clarify the potentially diverse mechanisms regulated by early T exposure across variable social environments. We additionally molecularly sexed the embryos to explore sex-specific effects. Overall design: Whole brains collected from embryos incubated to embryonic day 11 exposed to natural variation in maternal breeding density.

雌性个体对所处环境的行为与生理响应，会对子代发育产生持久影响。这类非遗传继承（或称母体效应，maternal effect）广泛存在于各类生物类群中，但在鸟类中研究得尤为深入——这是因为体外发育的鸟卵中，母体激素的测量相对简便。举例而言，在社会竞争强度较高的区域繁殖的雌性个体，会向卵黄中投入更多的睾酮（Testosterone，T）。这些暴露于高睾酮水平的子代将表现出多种表型改变：包括幼体生长速度加快、攻击性显著提升且该特性可持续至成年，而这类特征在高竞争环境中具备潜在适应性优势。据此推测，雌性个体可向子代传递当前所处的社会环境信息，帮助子代提前适应不利的生存条件。然而，母体激素如何作用于子代的近端机制，目前仍鲜有研究，这阻碍了我们对这一具有重要生态学意义的表型可塑性（phenotypic plasticity）来源的认知。本研究针对雌雄双色树燕（Tree Swallow，Tachycineta bicolor）胚胎，探讨了母体社会环境对卵黄睾酮分配以及全脑神经基因表达模式的影响。我们以繁殖位点密度存在自然差异的自由栖息双色树燕种群为研究对象，通过行为观测记录了各繁殖位点的身体攻击发生频率，结果显示高密度位点的攻击频率显著更高。我们在两个发育时间点采集卵样：产卵当日采集的卵用于检测母体源性睾酮浓度；胚胎发育第11天（ED11）采集的卵则通过RNA-seq（RNA测序）分析全脑的基因表达模式。本研究采用全基因组分析策略，旨在阐明不同社会环境下，早期睾酮暴露所调控的潜在多样化分子机制。此外，我们还通过分子生物学方法对胚胎进行性别鉴定，以探究睾酮效应的性别特异性差异。实验整体设计：采集暴露于自然梯度母体繁殖密度、且发育至胚胎第11天的胚胎全脑样本。