Collaborative Research: Comparative Genomics of Host-specific Adaptation and Life History Evolution of Brood Parasitic Birds

趋同进化的例子，其中相似的形态、行为或功能特征在不同物种中独立出现，提供了一个强大的框架，用于检查适应性进化背后的遗传变化在多大程度上是可预测的，而不是特殊的，这是比较基因组学的一个基本问题。鸟类巢寄生鸟类不向其后代提供亲代照顾，而是将卵产在其他物种的巢中，代表了比较分析的理想模型系统，因为巢寄生（以及亲代照顾行为的丧失）在五个不同的鸟类科中独立进化了七次。该项目将表征寄生和非寄生鸟类的基因组变化模式，以测试相同特定基因的变化和/或基因组变化的平行模式是否发生在独立的寄生谱系中。研究结果还将深入了解有关基因组进化的其他基本问题，包括行为差异背后的遗传变化是否最常见于基因组的调节部分，或者是否代表基因本身的结构变化。在第二个相关的调查中，该项目将研究性别决定染色体的独特进化动力学，利用最近的研究表明，利用特定宿主物种的专门适应是母系遗传的（从母亲传给女儿），因此在三种不同的巢寄生物种的鸟类 W 染色体（类似于人类 Y 染色体）上进行编码。该项目还将有助于培训各个职业阶段的科学家，包括本科生、研究生和博士后。本科生研究经历（REU）部分将为东卡罗来纳大学的两名学生提供在哈佛大学接受生物信息学培训的机会。该项目将为其他鸟类产生高质量的基因组组装，支持对脊椎动物基因组进化的额外比较分析，并且该项目的数据将被整合到支持分子和群体基因组学新兴领域课程的教育材料中。禽类寄生虫及其宿主表现出行为、形态和生理适应和反适应的惊人多样性，已成为共同进化研究的重要模型。最近在三种不同寄生物种中发现了遗传上不同的宿主特异性母系，这是“无需重组的适应”的例子，为研究选择对非重组、性别限制染色体的影响提供了一个独特的机会。同样，由于专性寄生有七个独立的起源以及相关的父母照顾的丧失，巢寄生生物为探索主要生活史转变的全基因组后果提供了无与伦比的机会，为基因组趋同测试提供了比最近其他表型趋同的基因组基础分析更大的力量。该研究的结果将有助于深入了解有关基因组进化的基本问题，包括决定论与历史偶然性的相对重要性，以及遗传网络的整合与模块化如何限制自然选择的结果。除了增加鸟类高质量基因组组装的数量（目前仅适用于斑胸草雀和鸡）和组装W染色体序列之外，拟议的研究还将测试两个主要假设：1）影响非重组、性别限制的W染色体的进化过程（例如希尔-罗伯逊干扰、选择性扫描、遗传搭便车）在具有母系遗传的宿主特异性适应性的寄生谱系中被放大； 2）检查所有七个寄生进化枝，巢寄生的进化（以及亲代照顾行为的丧失）导致全基因组分子趋同的特征和/或与特定遗传途径或功能相关的编码和/或调控区域的趋同变化。该奖项反映了 NSF 的法定使命，并通过使用基金会的智力价值和更广泛的影响审查标准进行评估，被认为值得支持。

Examples of convergent evolution, in which similar morphological, behavioral or functional traits arise independently in different species, provide a powerful framework for examining the extent to which the genetic changes underlying adaptive evolution are predictable versus idiosyncratic, a fundamental question in comparative genomics. Avian brood parasites, birds that provide no parental care to their offspring but instead lay their eggs in the nests of other species, represent an ideal model system for comparative analysis because brood parasitism (and the loss of parental care behavior) evolved independently seven times in five different avian families. This project will characterize patterns of genomic change in both parasitic and non-parasitic birds to test whether changes in the same specific genes and/or parallel patterns of genomic change have occurred in independent brood parasitic lineages. The results will also provide insight into other fundamental questions about genome evolution, including whether genetic changes underlying differences in behavior are most often in regulatory portions of the genome or represent structural changes to the genes themselves. In a second, related line of inquiry, the project will examine the unique evolutionary dynamics of the sex-determination chromosomes, leveraging recent research showing that specialized adaptations for exploiting particular host species are maternally inherited (passed from mother to daughter) and therefore encoded on the avian W-chromosome (analogous to the human Y-chromosome) in three different brood parasitic species. The project will also contribute to the training of scientists at various career stages including undergraduates, graduate students, and a postdoctoral fellow. A research experience for undergraduates (REU) component will provide an opportunity for two students from East Carolina University to receive training in bioinformatics at Harvard University. The project will produce high quality genome assemblies for additional bird species, supporting additional comparative analyses of genome evolution across vertebrates, and data from the project will be integrated into educational materials supporting courses in the emerging fields of molecular and population genomics.Avian brood parasites and their hosts, which exhibit a spectacular diversity of behavioral, morphological and physiological adaptations and counter-adaptations, have served as important models for the study of coevolution. Recent discoveries of genetically divergent, host-specific matrilines within each of three different parasitic species, examples of "adaptation without recombination", present a unique opportunity to examine the effects of selection on the non-recombining, sex-limited chromosome. Likewise, with seven independent origins of obligate parasitism and associated loss of parental care, brood parasites offer an unparalleled opportunity to explore the genome-wide consequences of a major life history transition, providing greater power for tests of genomic convergence than in other recent analyses of the genomic basis of phenotypic convergence. Results of the study will lend insight into basic questions about genome evolution, including the relative importance of determinism versus historical contingency, and the manner in which integration versus modularity of genetic networks constrains the outcomes of natural selection. In addition to increasing the number of high quality genome assemblies for birds (currently available for only zebra finch and chicken) and assembling W-chromosome sequences, the proposed study will test two major hypotheses: 1) that evolutionary processes influencing the non-recombining, sex-limited W-chromosome (e.g., Hill-Robertson interference, selective sweeps, genetic hitchhiking) are amplified in parasitic lineages that have maternally inherited host-specific adaptations; and 2) examining all seven parasitic clades, that the evolution of brood parasitism (and loss of parental care behavior) results in genome-wide signatures of molecular convergence and/or convergent changes in coding and/or regulatory regions associated with particular genetic pathways or functions.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.