Speciation patterns and evolutionary history of leaf-cutting ants and their obligate social parasites: an integrative phylogenomic approach

通过物种形成了解生物多样性的起源和维持是进化生物学的重点。异域物种形成，即由于地理隔离而导致的物种分化，被普遍接受。相比之下，同域物种形成，即物种在没有地理隔离的情况下的分化，是有争议的。目前的争论集中在同域物种形成对生物多样性起源的相对贡献和潜在的遗传机制上。同域物种形成已被反复提出在社会寄生的起源中发挥作用，但这尚未得到全面的验证。真菌农蚁是研究这一过程的理想模型系统。被研究的蚂蚁群居寄生虫没有工蚁等级，也不参与维持蚁群的任务。相反，它们专门利用宿主群体的资源来最大化自己的繁殖。群居寄生似乎是一种非常成功的生命史策略，因为群居寄生在蚂蚁身上已经独立进化了100多次。因此，这些蚂蚁代表了一系列独特的自然实验，允许测试物种形成模式，在比较背景下研究物种形成过程的遗传条件，并测试有关进化，生态和社会寄生行为的特定假设。为了充分利用这一研究系统，将重建形成丰富的宿主-寄生虫相互作用马赛克的进化史，并明确切叶蚁的物种边界。在实际层面上，这将使人们能够更好地识别这些经常遇到的、经济上非常重要的蚂蚁物种，这对农业研究人员和有害生物管理很重要。此外，通过研究类似的自然系统，该项目对改善人类农业和疾病管理具有实际影响。该项目将培养高中生、本科生、研究生和一名博士后研究员。在项目过程中，史密森尼国家自然历史博物馆将为国内外观众设计和实施一项关于切叶蚁和种植真菌蚁的研究的公共推广体验。该项目将采用系统基因组学、种群遗传学、行为学和分类学的综合方法来实现以下研究目标：(i)系统基因组学标记，即所谓的超保守元件（UCEs），将用于推断真菌养殖蚂蚁的全面的、化石校准的分子系统发育。系统发育学将被用来测试这六种群居寄生虫是否独立进化，寄生虫是否与它们的宿主是最近的亲戚，以及所谓的“早期”寄生虫是否比形态衍生的寄生虫进化得更晚。（ii）除了蚂蚁之外，我们将利用研究人员最近为真菌目Agaricales开发的UCE系统基因组标记，重建由切叶蚂蚁及其近亲培养的共生真菌的系统发育，这些真菌共同构成了所谓的“高等蚂蚁农业”。罕见的转向新的真菌品种可能与蚂蚁物种形成有关，因此真菌关联在蚂蚁物种形成过程中的可能作用将被测试。（iii）将采用综合方法，结合系统基因组学、种群遗传学和形态学数据，对切叶蚁属Atta和Acromyrmex进行分类修订和重新分类，包括卫星寄生虫Pseudoatta属。一个相互照明的过程将被应用于清晰地划定物种边界和识别隐蔽物种。对切叶蚁（其中一些是拉丁美洲严重的农业害虫）的物种边界的清楚了解将允许明确的物种识别并为有针对性的害虫管理策略提供信息。

Understanding the origin and maintenance of biological diversity via speciation is a priority in evolutionary biology. Allopatric speciation, the divergence of species resulting from geographical isolation, is universally accepted. In contrast, sympatric speciation, the divergence of species in the absence of geographical isolation, is controversial. The current debate focuses on the relative contribution of sympatric speciation to the origin of biodiversity in general and on the underlying genetic mechanisms. Sympatric speciation has been repeatedly suggested to play a role in the origin of social parasitism, but this has not been comprehensively tested. Fungal farming ants are an ideal model system to study this process. The ant social parasites to be studied lack a worker caste and do not contribute to colony maintenance tasks. Instead they are specialized on using the host colony's resources to maximize their own reproduction. Social parasitism appears to be a highly successful life-history strategy, given that social parasites have evolved more than 100 times independently and convergently in ants. Thus, these ants represent a unique series of natural experiments that allow for testing speciation patterns, for studying the genetic conditions underlying speciation processes in a comparative context, and for testing specific hypotheses regarding the evolution, ecology, and behavior of social parasitism. To take full advantage of this study system, the evolutionary history that shaped the rich mosaic of host-parasite interactions will be reconstructed and species boundaries in the leaf-cutting ants will be clearly delimited. On a practical level, this will enable the better identification of these commonly encountered and economically highly important ant species, which is important to agricultural researchers and pest management. Additionally, this project has real ramifications for the improvement of human agriculture and disease management through the study of an analogous natural system. This project will train high school students, undergraduates, graduate students and a post-doctoral researcher. In the course of the project a public outreach experience featuring this research on leaf-cutting ants and fungus-farming ants in general will be designed and implemented at the Smithsonian National Museum of Natural History for a national and international audience. This project will employ an integrative phylogenomic, population genetic, behavioral, and taxonomic approach to achieve the following research goals: (i) Phylogenomic markers, so-called ultra-conserved elements (UCEs), will be employed to infer a comprehensive, fossil-calibrated molecular phylogeny for the fungus-farming ants. The phylogeny will be used to test whether the six social parasite species evolved independently, whether parasites are the closest relatives of their hosts, and whether so-called "incipient" parasites evolved more recently than morphologically derived parasites. (ii) In addition to the ants, we will reconstruct the phylogeny of the symbiotic fungi cultivated by the leaf-cutting ants and their close relatives that together comprise so-called "higher ant agriculture" utilizing UCE phylogenomic markers that the researchers have recently developed for the fungal order Agaricales. Rare shifts to new fungal cultivars can be associated with ant speciation, and therefore the possible role of fungal association in the ant speciation process will be tested. (iii) An integrative approach, incorporating phylogenomic, population genetic, and morphological data, will be utilized to taxonomically revise and reclassify the leaf-cutting ant genera Atta and Acromyrmex, including the satellite parasite genus Pseudoatta. A process of reciprocal illumination will be applied to clearly delineate species boundaries and recognize cryptic species. A clear understanding of species boundaries in leaf-cutting ants, some of which are serious agricultural pests in Latin America, will allow for unambiguous species identification and inform targeted pest management strategies.