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

切叶蚁及其专性社会寄生虫的物种形成模式和进化史：综合系统发育学方法

• 批准号: 1654829
• 负责人: Christian Rabeling
• 金额: $ 87.89万
• 依托单位: Arizona State University
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2017
• 资助国家: 美国
• 起止时间: 2017-08-15 至 2021-07-31
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1654829&HistoricalAwards=false
• 关键词: Speciation; patterns; evolutionary; history; leaf

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.

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优先事项。异域物种形成，即由于地理隔离而导致的物种分化，已被普遍接受。与此相反，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以及潜在的遗传机制上。同域物种形成已被多次提出在社会寄生的起源中发挥作用，但这还没有得到全面的检验。真菌养殖蚂蚁是研究这一过程的理想模式系统。要研究的蚂蚁社会寄生虫缺乏一个工人种姓，不有助于殖民地的维护任务。相反，它们专门利用宿主殖民地的资源来最大限度地繁殖自己。社会寄生似乎是一种非常成功的生活史策略，因为社会寄生虫在蚂蚁中已经独立和收敛地进化了100多次。因此，这些蚂蚁代表了一系列独特的自然实验，可以测试物种形成模式，在比较的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，形成丰富的马赛克主机-寄生虫相互作用的进化历史将被重建和切叶蚁的物种边界将被明确划定。在实践层面上，这将有助于更好地识别这些常见且经济上非常重要的蚂蚁物种，这对农业研究人员和害虫管理非常重要。此外，该项目通过研究类似的自然系统，对改善人类农业和疾病管理产生了真实的影响。该项目将培养高中生、本科生、研究生和一名博士后研究员。在该项目的过程中，将在史密森尼国家自然历史博物馆为国内外观众设计和实施一个以切叶蚁和真菌养殖蚁研究为特色的公共推广体验。该项目将采用综合的昆虫基因组学、种群遗传学、行为学和分类学方法，以实现以下研究目标：（i）系统基因组标记，即所谓的超保守元件（UCE），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。寄生虫发生学将用于测试六种社会寄生虫物种是否独立进化，寄生虫是否是其宿主的近亲，以及所谓的“初期”寄生虫是否比形态衍生的寄生虫进化得更近。(ii)除了蚂蚁之外，我们还将重建由切叶蚂蚁及其近亲培养的共生真菌的共生性，这些真菌共同构成了所谓的“高等蚂蚁农业”，利用研究人员最近为真菌目的Agaricales开发的UCE基因组标记。罕见的转移到新的真菌品种可以与蚂蚁物种形成，因此，蚂蚁物种形成过程中的真菌协会可能发挥的作用将进行测试。(iii)一个综合的方法，将昆虫的基因组，种群遗传学和形态学数据，将被用来分类学修订和重新分类切叶蚁属阿塔和Acromyrmex，包括卫星寄生虫属Pseudoatta。一个相互照明的过程将被应用于明确划定物种边界和识别神秘物种。切叶蚁是拉丁美洲的严重农业害虫，对切叶蚁的物种界限有清楚的了解将有助于明确物种识别，并为有针对性的害虫管理战略提供信息。

项目成果

The dacetine ant Strumigenys arizonica, an apparent obligate commensal of the fungus-growing ant Trachymyrmex arizonensis in southwestern North America

• DOI: 10.1007/s00040-018-0625-8
• 发表时间: 2018-08-01
• 期刊: INSECTES SOCIAUX
• 影响因子: 1.3
• 作者: Gray, K. W.;Cover, S. P.;Rabeling, C.
• 通讯作者: Rabeling, C.

A checklist of the non-leaf-cutting fungus-growing ants (Hymenoptera, Formicidae) from Colombia, with new biogeographic records

哥伦比亚非切叶真菌生长蚂蚁（膜翅目、蚁科）清单，附有新的生物地理记录

• DOI: 10.15560/16.5.1205
• 发表时间: 2020
• 期刊: Check list
• 影响因子: 0.4
• 作者: Mera-Rodríguez D, Serna F

Compositional heterogeneity and outgroup choice influence the internal phylogeny of the ants

• DOI: 10.1016/j.ympev.2019.01.024
• 发表时间: 2019-05-01
• 期刊: MOLECULAR PHYLOGENETICS AND EVOLUTION
• 影响因子: 4.1
• 作者: Borowiec, Marek L.;Rabeling, Christian;Ward, Philip S.
• 通讯作者: Ward, Philip S.

Evolution: Shape shifting parasites

进化：变形寄生虫

• DOI: 10.1016/j.cub.2020.07.010
• 发表时间: 2020
• 期刊: Current Biology
• 影响因子: 9.2
• 作者: Parker J, Rabeling C.

Biogeography of mutualistic fungi cultivated by leafcutter ants

切叶蚁培育的共生真菌的生物地理学

• DOI: 10.1111/mec.14431
• 发表时间: 2017
• 期刊: Molecular Ecology
• 影响因子: 4.9
• 作者: Mueller, Ulrich G.;Ishak, Heather D.;Bruschi, Sofia M.;Smith, Chad C.;Herman, Jacob J.;Solomon, Scott E.;Mikheyev, Alexander S.;Rabeling, Christian;Scott, Jarrod J.;Cooper, Michael
• 通讯作者: Cooper, Michael