The drivers of major transitions in mutualistic dependence

物种间的合作（互惠主义）在自然界是普遍存在的。物种之间的这种伙伴关系可以是非常不同的。互惠关系从物种之间的联系（兼性）到紧密的义务伙伴关系（将物种的命运捆绑在一起）各不相同。这些不同类型的互惠关系是什么时候进化或消失的？是什么让一个物种有义务地依赖另一个物种？为什么有些关系可以和平地解散，而在其他情况下，离婚却是死路一条？该项目旨在了解互惠依赖何时以及如何演变。要解决这一重大科学挑战，需要分析不同尺度上的互惠关系。我将使用三种主要方法来做到这一点。我的第一种方法将涉及绘制不同种类的动物/植物共生关系，在植物生命树中存在和缺失，以便了解它们何时进化或崩溃。为此，我将使用三种主要的动物/植物相互作用：授粉、种子传播和植物防御食草动物或病原体。这三种重要的生态类型的动物/植物互惠共生汇聚在一起，关键功能可以依赖或独立于动物互惠共生。我将把这些策略映射到一个大的进化植物树（系统发生学）上。这将允许我测试几个关于促进互惠依赖或其崩溃的因素的假设。我的下一个目标是确定基因构成中的哪些变化导致了相互依赖的转变。到目前为止，我们对这一领域的了解仅限于涉及宿主体内微生物的共生关系。我以前的工作表明，兼性互惠很容易丢失，而专性互惠是进化保守的。是什么定义了这些相互依赖的可逆性？为了解决这些问题，我将重点关注一种共生共生关系，即植物寄主蚂蚁以换取额外的营养（有时是防御食草动物）。这组来自咖啡科的约105种植物是回答这个问题的理想系统，因为它们有不同程度的依赖。利用DNA测序，我将关注三个主要问题：(1)在蚂蚁和植物之间的共生关系中，功能基因的缺失是否驱动了共生依赖，就像微生物和宿主之间的伙伴关系一样？(2)不同程度的相互依赖如何影响基因进化的速度？(3)在兼性依赖向专性依赖转变的过程中，我们能否确定与性状进化相关的基因组变化？最后，我将检验这一假设，即这一群体中对蚂蚁的强制性依赖是病原体防御功能丧失的结果（这意味着这种功能是由蚂蚁执行的），这是由我的初步数据产生的。为此，我将在现场进行实验，从专性和兼性植物中去除蚂蚁，并检查所有这些处理下的植物健康状况，特别是通过使用最先进的方法来比较这些不同情况下的微生物群落。反过来，这将揭示微生物群落相互依赖的影响。在这个项目结束时，我希望能够确定促进互惠依赖进化的条件，强制性依赖被介导的机制，以及它如何影响动物/植物互惠共生中基因组成的进化。由于互惠依赖影响了许多生态和进化过程，了解它是如何进化的将增强我们对物种进化的理解。此外，由于高度依赖、有义务的互惠主义者被认为更容易灭绝，因为他们的命运与他们的互惠伙伴联系在一起，这项研究有可能为保护提供信息。

Cooperation among species (mutualism) is widespread in nature. Such partnerships between species can be of very different kinds. Mutualisms vary from associations between species that can also live without each other (facultative) to tight obligate partnerships binding species' fates together. When do these different types of mutualisms evolve or get lost? What makes a species obligately dependent on another one? Why can some associations peacefully disassemble while, in other cases, divorce is a dead end? This project aims to understand when and how mutualistic dependence evolves. Addressing this major scientific challenge requires analysing mutualistic associations at different scales. I will do so using three main approaches. My first approach will involve mapping different kinds of animal/plant mutualisms presence and absence across the plant tree of life in order to understand when they evolve or break down. To do this, I will use three major animal/plant mutualisms: pollination, seed dispersal and plant defence against herbivores or pathogens. These three ecologically important types of animal/plant mutualisms converge in that the key function can be dependent or independent on an animal mutualism. I will map these strategies on a large evolutionary plant trees (phylogenies). This will allow me to test several hypotheses regarding the factors promoting mutualistic dependence or its breakdown.My next goal will be to determine what changes in the genetic makeup are responsible for shifts in mutualistic dependence. So far, our knowledge on this area is restricted to mutualisms involving microbes living inside a host. My previous worked has shown that facultative mutualisms are lost easily while obligate mutualisms are evolutionary conserved. What defines the reversibility of these mutualistic dependencies? To address these questions, I will focus on a type of symbiotic mutualisms where plants host ants in return for extra nutrients (and sometimes defence against herbivores). This group of ~105 plant species from the coffee family is ideal system to answer this question since they have various levels of dependence. Using DNA sequencing, I will focus on three main questions: (1) Does the loss of functional genes drive mutualism dependence in these symbioses between ants and plants, as it does in partnerships between microbes and hosts? (2) How do different levels of mutualistic dependence affect the pace of gene evolution? And (3) Can we identify the genomic changes associated with trait evolution in the transition from facultative to obligate dependence?Finally, I will test the hypothesis that obligate dependence on ants in this group is the result of the loss of pathogen defence function (implying that this function is performed by the ants), which arises from my preliminary data. To do so, I will perform experiments in the field where I remove ants from obligate and facultative plants, and examine plant heath across all these treatments, notably by using a state-of-the-art method to compare microbes communities in these different cases. This will, in turn, reveal the impact of mutualistic dependence on microbial communities.At the end of this project, I hope to have identified the conditions fostering the evolution of mutualistic dependence, the mechanisms by which obligate dependence is mediated and how it impacts the evolution of the genetic makeup in an animal/plant mutualism. Since mutualistic dependence affects many ecological and evolutionary processes, understanding how it evolves will enhance our understanding of species evolution. Moreover, because highly dependent, obligate mutualists are deemed to be more vulnerable to extinction since their fate is bound to their mutualistic partner, this research has the potential to inform conservation.