EDGE CMT: Origin and diversification of butterfly color patterns

EDGE CMT：蝴蝶色彩图案的起源和多样化

• 批准号: 2128164
• 负责人: Robert Reed
• 金额: $ 139万
• 依托单位: Cornell University
• 依托单位国家: 美国
• 项目类别: Continuing Grant
• 财政年份: 2021
• 资助国家: 美国
• 起止时间: 2021-08-15 至 2025-07-31
• 项目状态: 未结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=2128164&HistoricalAwards=false
• 关键词: EDGE; CMT; Origin; diversification; butterfly

When we look across the diversity of life, we see many complex traits that are unique to certain groups of organisms. Feathers in birds, hair in mammals, and flowers in angiosperms, for example. It is a major question in biology how these kinds of novel traits first appear. What is the genetic basis of newness? Recent work across many species has shown that novel traits such as these are largely generated by old genes that have been repurposed for new roles. Novelty appears to emerge through a reshuffling of older genetic building blocks, which are proposed to be ancient subnetworks of interacting genes. But where do these gene networks come from in the first place? And how are they rewired to generate complex new traits? With this funding, Reed and colleagues are beginning to address these questions by looking at the origin of color in butterflies. They are characterizing the gene networks that underlie color pigmentation in butterflies, and they are determining how specific genetic changes caused these networks to be repurposed from ancestral roles in processes such as neural development, to make butterfly wing patterns. This work serves as a case study to help biologists understand the developmental genetic mechanisms that underlie the genesis and diversification of complex biological traits. The project also includes training in biology research skills of graduate and undergraduate students from diverse backgrounds, the development and dissemination of instructional videos for genomic methods, and the establishment of a web-based resource for functional genomics in butterflies.A core concept in modern biology is that novel morphological traits originate from gene regulatory networks that predate the traits themselves. Surprisingly, however, little is known about the specific genetic mechanisms that underlie the origin and repurposing of such gene networks. With this funding, Reed and colleagues develop the regulatory network encompassing the butterfly color pattern gene optix into a model for exploring the regulatory architecture of trait diversification. optix is a homeobox transcription factor that plays a deeply ancestral role in neural and retinal development in both invertebrates and vertebrates. In butterflies, however, this gene underwent a radical co-option event where it gained a novel function as a master regulator of wing pigmentation, including playing key roles in adaptation and mimicry. Thus, the researchers have a situation in Lepidoptera where they can pinpoint the phylogenetic timing of a major optix co-option and repurposing event, where this gene appeared as a de novo regulator of color patterns. Reed and colleagues are leveraging this opportunity to take a multi-species comparative approach to characterize the history of the optix regulatory network as it gained its novel adaptive function in color pattern regulation. Using optix as the focal point, they are characterizing the cis-, upstream, and downstream regulatory dynamics of regulatory co-option, and construct a comprehensive case study of how a new gene regulatory network can emerge from the genome to generate new morphological features – in this case, color itself.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.

当我们纵观生命的多样性时，我们看到许多复杂的特征是某些生物群体所独有的。例如鸟类的羽毛，哺乳动物的毛发，被子植物的花。这是生物学中的一个主要问题，这些新的特征是如何首先出现的。新事物的遗传基础是什么？最近对许多物种的研究表明，诸如此类的新特征在很大程度上是由旧基因产生的，这些基因被重新利用以发挥新的作用。新奇的出现似乎是通过对旧的遗传构建块的重新洗牌，这些构建块被认为是相互作用的基因的古老子网络。但是这些基因网络最初是从哪里来的呢？它们又是如何重组以产生复杂的新特征的？有了这笔资金，里德和同事们开始通过研究蝴蝶颜色的起源来解决这些问题。他们正在描述蝴蝶色素沉着的基因网络，并确定特定的遗传变化如何导致这些网络从神经发育等过程中的祖先角色重新定位，以形成蝴蝶翅膀图案。这项工作作为一个案例研究，以帮助生物学家了解复杂的生物性状的起源和多样化的基础发育遗传机制。 该项目还包括来自不同背景的研究生和本科生的生物学研究技能培训，基因组方法教学视频的开发和传播，以及基于网络的蝴蝶功能基因组学资源的建立。现代生物学的一个核心概念是，新的形态特征起源于早于特征本身的基因调控网络。然而，令人惊讶的是，人们对这种基因网络的起源和再利用的特定遗传机制知之甚少。有了这笔资金，Reed及其同事开发了包含蝴蝶颜色模式基因optix的调控网络，并将其转化为探索性状多样化调控结构的模型。optix是一种同源框转录因子，在无脊椎动物和脊椎动物的神经和视网膜发育中起着非常古老的作用。然而，在蝴蝶中，这个基因经历了一个激进的共同选择事件，它获得了一个新的功能，作为翅膀色素沉着的主要调节者，包括在适应和模仿中发挥关键作用。因此，研究人员在鳞翅目中有一种情况，他们可以确定主要optix co-option和repurposing事件的系统发育时间，该基因作为颜色模式的从头调节器出现。Reed及其同事正在利用这个机会，采取多物种比较方法来描述Optix调节网络的历史，因为它在颜色模式调节中获得了新的适应功能。以optix为焦点，他们正在表征调控协同选择的顺式、上游和下游调控动力学，并构建一个全面的案例研究，研究新的基因调控网络如何从基因组中出现，以产生新的形态学特征--在这种情况下，该奖项反映了NSF的法定使命，并已被认为是值得通过评估使用基金会的知识支持。优点和更广泛的影响审查标准。

项目成果

High level of novelty under the hood of convergent evolution

• DOI: 10.1126/science.ade0004
• 发表时间: 2023-03-10
• 期刊: SCIENCE
• 影响因子: 56.9
• 作者: Belleghem, Steven M. Van;Ruggieri, Angelo A.;Papa, Riccardo
• 通讯作者: Papa, Riccardo

Deep cis-regulatory homology of the butterfly wing pattern ground plan

• DOI: 10.1126/science.abi9407
• 发表时间: 2022-10-20
• 期刊: SCIENCE
• 影响因子: 56.9
• 作者: Mazo-Vargas, Anyi;Langmueller, Anna M.;Reed, Robert D.
• 通讯作者: Reed, Robert D.