Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata)

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be via maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24 hr old eggs of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-hr-old eggs, which were past the maternal-zygote-transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.

母性效应是表型变异的重要来源，其中雌性通过直接遗传贡献之外的途径影响后代的发育轨迹，通常是对不断变化的环境条件的响应。然而，关于母性经验如何转化为塑造后代发育的分子信号的机制，我们所知甚少。其中一种信号可能是通过母性RNA转录本（mRNA和miRNA）沉积到成熟的卵母细胞中实现的。这些转录本调节所有动物的发育早期阶段，但在大多数昆虫中研究不足。在本研究中，我们调查了雌性内部（身体条件）和外部（季节时间）环境条件对紫花苜蓿叶切蜂成熟卵母细胞和24小时龄卵中母性RNA的影响。通过基因表达和WGCNA分析，我们发现雌性在面临较差的身体条件和伴随晚季的较短日照时间时，会调整沉积到成熟卵母细胞中的与蛋白质磷酸化、转录调控和核酸酶活性相关的mRNA数量。然而，这些变化的幅度在季节时间上更高。雌性还会根据季节变化调整miRNA的沉积，但不是根据身体条件。我们没有观察到在24小时龄卵中，无论是身体条件还是季节时间对母性RNA的显著变化，这些卵已经超过了母-配子体转换期。我们的结果表明，雌性通过调整提供给后代的RNA转录本以调节发育，对内部和外部环境线索作出反应。因此，母性RNA的变异性可能对于调节后代对环境变化的表型反应具有重要意义。