Cis-regulation and conditional chromatin remodeling in development and evolution of ontogenies in horned beetles

生命之树中的生物体会根据不同的内部和外部影响来调整它们的生长方式。同样的特征在雄性和雌性身上的表现可能不同，或者看起来不同，这取决于发育中的生物体是否能获得足够的食物。这种“有条件”或“环境响应”的发展是广泛存在的，并且在性状和物种之间迅速而极大地多样化。过去的工作确定了许多调节条件响应性发育的重要机制，然而，这些差异最初是如何产生的，以及随后的发展如何解释这些差异并相应地调整自身，仍然知之甚少。这项研究使用角甲虫作为研究系统来填补这一空白。角甲虫具有高度多样的环境响应性发展形式，可用于比较和实验研究。通过这个研究系统的镜头，这项工作旨在(a)表征遗传网络，该网络允许复杂特征的发展，如角、翅膀和腿，在响应不同的条件下启动和完成；以及(b)研究这种调节如何从性状到性状、从物种到物种的变化，从而有助于生物多样性。这项研究进一步整合到多方面的科学推广活动中，旨在开发支持K12印第安纳州科学教学标准的资源，培训K-12教师，并增加历史上代表性不足的人口对科学的参与。通过发育过程的中介，基因型和环境的整合形成了生物体的形态和功能。本研究将探讨角甲虫在个体发育过程中整合基因型和环境的发育机制，以及这种整合的变化如何影响该物种内部和物种之间的生物多样性。该研究将染色质可及性和基因表达的全基因组分析与候选基因和途径的功能分析相结合，将开辟新的领域。此外，这项工作将以比较的方式在其环境响应性发展的程度或性质不同的性状之间进行，并在性状特异性条件发展中出现分歧的物种之间进行。拟议的工作有三个主要目标：第一，它将确定顺式管理结构在环境和男性/女性特定发展中的作用。其次，它将描述这一角色如何在不同的分类群和特征中多样化，代表不同程度的进化多样化和创新。最后，本研究将评估几种已知的条件依赖性发育的主调控因子及其产生种内形态变异的环境响应性基因调控网络之间相互作用的性质，以及其中的进化变化。总的来说，提出的工作旨在改变我们对个体发育过程中生物形态和功能起源中基因型和环境整合的发育机制的理解，以及这种整合的变化如何影响物种内和物种间的生物多样性。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Organisms across the tree of life adjust the way they grow in response to diverse internal and external influences. The same traits may manifest differently in males compared to females, or look different depending on whether the developing organism had access to sufficient food or not. Such “conditional” or “context-responsive” development is wide-spread, and has diversified rapidly and greatly across traits and species. Past work identified many important mechanisms that regulate condition-responsive development, yet, how such differences arise in the first place, and how subsequent development interprets these differences and adjusts itself accordingly, remains very poorly understood. This research uses horned beetles as a study system to fill this void. Horned beetles possess highly diverse forms of context-responsive development that are amenable to comparative and experimental study. Through the lens of this study system this work aims to (a) characterize the genetic networks that allows the development of complex traits such as horns, wings, and legs to be both initiated and completed in response to varying conditions; as well as (b) investigate how this regulation changes from trait to trait, and from species to species, and thereby contributes to organismal diversity. This research is further integrated within multifaceted science outreach activities aimed at developing resources in support of K12 Indiana Science Teaching Standards, training K-12 teachers, and increasing the participation of historically underrepresented demographics in science. Organismal form and function emerge through the integration of genotype and environment via the agency of developmental processes. The proposed work will address the developmental mechanisms by which the horned beetle species Onthophagus integrates genotype and environment in the genesis of organismal form and function during ontogeny, and how changes in this integration shape organismal diversity both within and among this species. This research will break new ground by integrating the genome-wide analysis of chromatin accessibility and gene expression with the functional analysis of candidate genes and pathways. Further, this work will be executed in a comparative manner across traits that differ in the degree or nature of their context-responsive development, and across species that have diverged in trait-specific conditional development. The proposed work has three major objectives: first, it will identify the role of cis-regulatory architecture in environment- and male/female-specific development. Second, it will characterize how this role has diversified across taxa and traits representing varying degrees of evolutionary diversification and innovation. Finally, this research will assess the nature of interactions – as well as evolutionary changes therein – between several known master-regulators of condition-dependent development and their context-responsive gene regulatory networks in producing intraspecific morphological variation. Collectively, the proposed work aims to transform our understanding of the developmental mechanisms that integrate genotype and environment in the genesis of organismal form and function during ontogeny, and how changes in this integration shape organismal diversity both within and among species.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.