The Bio- and Phylogeography of Sympatric Speciation in Rhagoletis

研究的知识和科学焦点集中在如何形成新种类的pomonella果蝇。物种形成发生在种群之间基因流动的遗传屏障的进化过程中，这种屏障导致它们在繁殖上彼此隔离。传统上，物种形成被认为要求种群在地理上完全被移动的物理障碍（如山脉、大河、海洋）隔离。地理隔离使个体无法在种群之间移动，从而导致种群之间独立发生遗传变化，随着时间的推移，这些变化可能累积到种群进化成生殖隔离的物种的程度。然而，苹果蛆蝇（Rhagoletis pomonella）一直被认为是一个可能的例外。早在1864年，本杰明·沃尔什（Benjamin Walsh）就假设，某些专门攻击特定植物的昆虫在迁移和生态适应新寄主植物的过程中，可以在没有地理隔离的情况下（“同属”）形成物种。沃尔什特别提到了19世纪50年代发生在美国的一件事，即pomonella从其原生寄主植物山楂（山楂属）转移到引进的驯化苹果树上，这是他的同域物种形成理论的一个实时例子。随后的基因研究证实了沃尔什的假设，即寄生于苹果和山楂的pomonella Rhagoletis是部分繁殖隔离的“宿主种族”，可能处于分化成新物种的第一阶段。造成苹果和山楂蝇分化的一个重要因素是，苹果和山楂树在一年中的不同时间结果，导致苹果和山楂蝇每年一代的生命周期必须抵消，以便它们能够攻击苹果和山楂树。最近，Rhagoletis的故事有了一个有趣的转折。导致美国苹果蝇和山楂蝇生活史差异的一些基因可能起源于100多万年前墨西哥一个孤立的山楂蝇种群。这些基因在遥远的过去被引入美国，当时墨西哥和美国的山楂蝇种群接触（大约50万年前），最近这些基因帮助促进了欧洲殖民者在美国种植苹果后向驯化苹果的转变。因此，地理隔离和基因流动可能与生态专门化相结合，有助于触发“同域”物种形成事件（例如，苹果引入美国为山楂蝇提供了一个新的生态位——一个暂时的资源岛——它们能够利用这个生态位，部分原因是它们由于过去来自墨西哥的基因流动而拥有的遗传变异）。目前的拨款提案将通过对横纹肌蝇基因组中基因DNA序列的广泛分析来验证这一生物地理学假说。这项研究将包括对墨西哥各地收集的苍蝇进行调查，以确定该国Rhagoletis苍蝇的地理范围，并查明过去流入美国的基因可能的来源。此外，基因分析将表明某些基因和基因组区域是否具有使它们更容易或更不容易进入美国苍蝇种群的特征（例如，基因是否存在于倒位-染色体的延伸，它们具有不同的基因线性顺序-这被假设为阻碍物种之间的基因流动）。通过这种方式，这项研究将解决苹果侵染的新形式pomonella Rhagoletis最近转变和形成的遗传历史。这项研究的广泛影响和社会效益是多方面的。该项目将整合地方、社区、大学和国际层面的科学培训和教育活动。该研究将涉及博士后助理、研究生、本科生和高中生的参与，从实地和实验室研究到课堂模块，旨在为高中生和教育工作者提供分子遗传技术和分析的实践经验。目前提案提供的资金也将扩大和加强处于发展关键阶段的圣母大学人口生物学项目。此外，这项拟议的研究代表了圣母大学的研究人员与韦拉克鲁斯州哈拉帕生态研究所的两位杰出的墨西哥同事马丁·阿卢贾博士和胡安·鲁尔博士之间的国际合作。Drs。Aluja和Rull也得到了CONACyT的平行支持，以资助这项合作。最后，提出的Rhagoletis研究具有重要的应用和基础科学意义。pomonella Rhagoletis pomonella是苹果的主要经济害虫，其相关物种会攻击樱桃、蓝莓和其他几种作物。墨西哥褐毛鼠的范围和寄主范围问题对两国之间的水果进出口以及如何形成和控制新的有害物种种群具有重要影响。因此，拟议研究的影响范围从新的基础和应用科学发现，到教育和社会效益。

The intellectual and scientific focus of the research centers on how new species of Rhagoletis pomonella fruit flies form. Speciation occurs as genetic barriers to gene flow evolve between populations that cause them to become reproductively isolated from one another. Traditionally, speciation has been thought to require that populations be completely geographically isolated by physical barriers to movement (e.g., mountain ranges, large rivers, oceans). By precluding individuals from moving between populations, geographic isolation results in genetic changes occurring independently between populations which, over time, can accumulate to the point that the populations evolve into reproductively isolated species. The apple maggot fly, Rhagoletis pomonella, has been argued to be a possible exception, however. As early as 1864, Benjamin Walsh hypothesized that certain insects that specialize on attacking specific plants could speciate without geographic isolation ("in sympatry") in the process of them shifting and ecologically adapting to new host plants. In particular, Walsh cited the shift of Rhagoletis pomonella from its native host plant hawthorn (Crataegus) to introduced, domesticated apple trees in the United States - an event that occurred in the 1850's - as a real time example of his idea of sympatric speciation in action. Subsequent genetic studies have confirmed Walsh's hypothesis that the apple and hawthorn-infesting forms of Rhagoletis pomonella are partially reproductively isolated "host races", potentially in the first stages of diverging into new species. An important factor responsible for the divergence of the apple and hawthorn flies is that apple and hawthorn trees fruit at different times of the year, resulting in the one-generation per year life cycles of apple and hawthorn flies having to be offset in order for them to be able to attack apple vs. hawthorn trees. Recently, an interesting twist to the Rhagoletis story has been discovered. Some of the genes responsible for the difference in the life history of apple and hawthorn flies in the United States may have originated over a million years ago in an isolated population of hawthorn-infesting flies in Mexico. These genes were introduced into the U.S. in the distant past during a period when the Mexican and US hawthorn-fly populations came into contact (perhaps 500,000 years ago), and very recently these genes helped facilitate the shift to domesticated apple following the planting of apples in the US by European colonists. Thus, geographic isolation and gene flow may act in conjunction with ecological specialization to help trigger "sympatric" speciation events (i.e., the introduction of apples into the U.S. provided hawthorn flies with a new ecological niche - a temporal resource island - that they were able to take advantage of, in part, because of the genetic variation they possessed due to past gene flow from Mexico). The current grant proposal will test this biogeographic hypothesis thorough an extensive analysis of DNA sequences of genes located throughout the genome of Rhagoletis flies. The research will involve a survey of flies collected throughout Mexico to determine the extent of the geographic range of Rhagoletis flies in the country and pinpoint possible sources of gene flow into the U.S. in the past. In addition, the genetic analysis will indicated whether certain genes and genomic regions have characteristics that made them more or less prone to have moved into the US fly population (e.g., whether or not the genes reside within inversions - stretches of chromosomes that have different linear orders of genes along them - that have been hypothesized to retard gene flow between species). In this manner, the research will resolve the genetic history underlying the recent shift and formation of the new form of apple-infesting Rhagoletis pomonella. The broader impacts and societal benefits of the research are multifaceted. The project will integrate science training and educational activities at the local, community, University, and international levels. The study will involve the participation of a Post-Doctoral associate and graduate, undergraduate, and high school students in various aspects of the work ranging from field and laboratory research to class modules designed to give high school students and educators hands on experience with molecular genetic techniques and analysis. The funding provided by the current proposal will also expand and strengthen the Population Biology program at the University of Notre Dame at a critical stage of its development. In addition, the proposed research represents an international collaboration between researchers at Notre Dame and two distinguished Mexican colleagues, Dr. Martin Aluja and Dr. Juan Rull, at the Ecological Institute in Xalapa, Veracruz. Drs. Aluja and Rull have received parallel support from CONACyT to fund the collaboration. Finally, the proposed Rhagoletis research has significant applied, as well as basic, scientific implications. Rhagoletis pomonella is a major economic pest of apples, and related species attack cherries, blueberries, and several other crops. The question of the extent and host range of Rhagoletis pomonella in Mexico has important implications concerning the import and export of fruit between the two countries, as well as how new populations of pest species form and can be controlled. The impact of the proposed research is therefore ranges from new basic and applied scientific findings, to educational and societal benefits.