From Model Organism to Model Clade: Plasticity and Evolution of Interorgan Communication Networks

在自然界中观察到的发育和生理变化，不仅仅是基因差异的结果。大量数据现在表明，基因和环境(营养、致癌物质)共同产生了这种变异。蚂蚁是研究环境变化如何影响基因功能的新兴模型。蚂蚁是高度可塑性的：在发育过程中，同一组基因可以通过环境提示和激素调节产生一系列不同的表型。这在不同种姓的个体之间产生了巨大的差异，从形态、繁殖和寿命的差异都有。例如，环境变化可能会产生一只存活几个月的小型生殖不育工蚁，或者一只可以活到50岁的巨大的超生殖女王。从昆虫到哺乳动物，为了确保生理状态反映环境的动态条件，发育和成体器官都进化出信号(例如。小肽、激素和miRNAs)，构成器官间通讯网络。我的实验室的研究目标是研究在发育和成年期协调器官相互交流的分子信号，这是产生种姓特异性变异的关键。在这项工作的同时，我的实验室将使用遗传模型果蝇黑腹果蝇来研究这些信号的机械细节。通过利用新兴生物体和模式生物体，我的实验室将共同产生和解决具有基本生物学重要性的新问题，并提供高分辨率的机械细节。特别是，我们提出了以下三个短期目标/问题：(1)在发育过程中，种姓特定的荷尔蒙差异如何影响器官生长和形态发生的调节，以及随后如何导致发育中器官分泌的信号的种级差异？(2)在成年期，蚁后和工蚁之间生殖能力的巨大差异如何影响各种非生殖器官的功能和信号传递？(3)在进化过程中，这些不同的发育和成年种姓轨迹是如何起源的，从而使不同蚂蚁观察到的形态和生理特征存在巨大差异。我们的方法是高度集成的，结合了田野调查、系统发育学、功能基因组学、转录组学、发育遗传学、细胞和组织培养以及先进的显微技术。我们还整合了从基因网络和细胞到个人和社会的各种生物学水平，并将把稳健的相对多物种的模型分支方法(ANTS)与高分辨率的机械模型生物体方法(FOLS)协同工作。总之，它将促进我们了解器官间信号如何在发育、生理和进化的背景下，在不断变化的环境中调节有机体的反应。

Developmental and physiological variation observed in nature, is not the result of differences in genes alone. A wealth of data now demonstrates that genes and the environment (nutrition, carcinogens) together generate this variation. Ants are an emerging model to investigate how environmental variation influences gene function. Ants are highly plastic: during development, the same set of genes can give rise to an array of alternative phenotypes through environmental cues and hormonal regulation. This generates dramatic differences between individuals of different castes, ranging from differences in morphology, reproduction, and longevity. For example, environmental variation can generate a small reproductively sterile worker that lives for a few months or a massive hyper-reproductive queen that can live up to 50 years. From insects to mammals, to ensure that physiological status reflects the dynamic conditions of the environment, developing and adult organs have evolved signals (ex. small peptides, hormones, and miRNAs) that comprise an interorgan communication network. The research goal of my laboratory is to investigate the molecular signals coordinating the intercommunication of organs during both development and adulthood, which are critical for generating caste-specific variation. In parallel to this work, my laboratory will investigate these signals in mechanistic detail using the genetic model fruit fly Drosophila melanogaster. Collectively by leveraging both emerging and model organisms, my laboratory will generate and tackle novel questions of fundamental biological importance with high-resolution mechanistic detail. In particular, we set out address the following three short-term objectives/questions: (1) During development, how do caste-specific hormonal differences influence the regulation of organ growth and morphogenesis, and subsequently how does this lead to caste differences in signals secreted by developing organs? (2) During adulthood, how do dramatic differences in reproductive capacity between queens and workers impact the functionality of, and signaling between, various non-reproductive organs? (3) During evolution, how have these divergent developmental and adult caste trajectories originated, enabling the vast diversity of morphological and physiological traits observed across ants. Our approach is highly integrative combining fieldwork, phylogenetics, functional genomics, transcriptomics, developmental genetics, cell and tissue culture, and advanced microscopy techniques. We also integrate various biological levels spanning from gene networks and cells, to individuals and societies, and will synergize a robust comparative multispecies `Model Clade' approach (ants) with a high-resolution mechanistic model organism approach (flies). Altogether, it will advance our knowledge of how interorgan signaling mediates the response of an organism in a changing environment in the context of development, physiology, and evolution.