Mechanisms promoting speciation with gene flow in host-specialized haplodiploids

进化生物学中持续时间最长的争论之一是新物种能否在相互交换基因的过程中形成。基因交换被认为使物种形成变得困难，因为它混合了遗传背景。这种混合防止了物种间差异的积累。然而，基因数据告诉我们，自然界中许多物种确实交换基因。这个项目的目标是了解一些物种是如何经受住基因交换的。为此，该项目将重点放在一对以松树为食的昆虫物种上，它们是美国东部常见的害虫。这两个物种适应了不同的松树物种，并在它们的历史中交换了基因。通过关注未成熟阶段和成年阶段以及两性，该项目将更全面地了解适应不同环境如何产生新物种。通过填补我们对新物种如何产生的理解空白，这项工作将加深我们对周围世界的理解。这些知识将有助于我们保护生物多样性和防治害虫。此外，研究人员将利用他们的项目开发教育材料，向一年级的生物学学生教授遗传学和进化论。该项目还将为数十名学生提供参与真实科学研究的机会。这样的经历可以帮助我们留住STEM学科的优秀学生。进化理论预测，基因流动的物种形成是困难的，但经验数据表明，这种分化情景在自然界是常见的。为了调和这些看似矛盾的发现，拟议的工作利用了实验上可处理的一对松锯蝇物种（Neodiprion lecontei和N. pinetum），它们适应不同的松树，具有特殊的基因组资源，广泛的互补数据和基因流的分歧历史。首先，将利用焦点物种的幼虫饮食操纵及其相互的雄性和雌性杂交种来量化所有寄主植物组合的生殖隔离，并评估表型可塑性在促进基因流动的物种形成中的作用。其次，将利用这两个物种及其在两个亲本宿主上饲养的互惠第一代杂交种的幼虫转录组来揭示对幼虫饮食的不同转录反应如何促进宿主适应和杂交种的基因错误表达。第三，将利用在两个亲本宿主上饲养的第二代杂交雄虫的数量性状位点定位来描述寄主依赖性和寄主非依赖性杂交雄虫的生存能力、幼虫性能和成虫形态的遗传结构。由于这项工作为表型变异的复杂性和自然选择产生新物种的机制提供了直观的例子，因此拟议工作的数据将用于开发案例研究和科学家聚光灯，用于生物学入门课程，并为学生驱动的研究提供动力。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。

One of the longest running debates in evolutionary biology is whether new species can form while exchanging genes with one another. Gene exchange is thought to make species formation difficult because it mixes up genetic backgrounds. This mixing prevents the buildup of differences between species. Nevertheless, genetic data tell us that many species do exchange genes in nature. The goal of this project is to understand how some species can withstand gene exchange. To do so, this project focuses on a pair of pine-feeding insect species that are common pests in the eastern United States. These two species are adapted to different pine species and have exchanged genes throughout their history. By focusing on immature and adult life stages and both sexes, this project will produce a more complete picture of how adaptation to different environments produces new species. By filling gaps in our understanding of how new species arise, this work will deepen our understanding of the world around us. This knowledge will help us preserve biodiversity and combat pests. Additionally, the researchers will use their project to develop educational materials for teaching genetics and evolution to first-year Biology students. This project will also provide opportunities for dozens of students to participate in authentic scientific research. Such experiences can help us retain talented students in STEM disciplines. Evolutionary theory predicts that speciation with gene flow is difficult, yet empirical data indicate such divergence scenarios are common in nature. To reconcile these seemingly contradictory findings, the proposed work takes advantage of an experimentally tractable pair of pine sawfly species (Neodiprion lecontei and N. pinetum) that are adapted to different pines and have exceptional genomic resources, extensive complementary data, and a history of divergence with gene flow. First, larval diet manipulations of the focal species and their reciprocal male and female hybrids will be used to quantify reproductive isolation on all combinations of host plants and to evaluate the role of phenotypic plasticity in promoting speciation with gene flow. Second, larval transcriptomes of the two species and their reciprocal first-generation hybrids reared on both parental hosts will be used to uncover how divergent transcriptional responses to larval diet contribute to host adaptation and gene misexpression in hybrids. Third, quantitative trait locus mapping in second-generation hybrid males reared on both parental hosts will be used to describe the genetic architecture of host-dependent and host-independent hybrid viability, larval performance, and adult male morphology. Because this work provides intuitive examples of the complexity of phenotypic variation and mechanisms through which natural selection produces new species, data from the proposed work will be used to develop a case study and scientist spotlights for use in introductory Biology courses and to fuel student-driven research.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.