The drivers of major transitions in mutualistic dependence

物种间的合作（互利共生）在自然界中广泛存在。物种之间的这种伙伴关系可以是非常不同的类型。互利主义从物种之间的关联，也可以生活在没有对方（兼性），以紧密的强制性伙伴关系绑定物种的命运在一起。这些不同类型的互惠关系是什么时候进化或消失的？是什么让一个物种必须依赖另一个物种？为什么有些协会可以和平解散，而在其他情况下，离婚是一条死胡同？该项目旨在了解互惠依赖何时以及如何演变。应对这一重大科学挑战需要分析不同尺度的互惠关系。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/植物互惠关系，在植物生命树中存在和不存在，以便了解它们何时进化或分解。为了做到这一点，我将使用三个主要的动物/植物互惠：授粉，种子传播和植物防御食草动物或病原体。这三种生态学上重要的动物/植物互惠共生类型汇聚在一起，其关键功能可以依赖于或独立于动物互惠共生。我将把这些策略映射到一个大型的进化植物树（进化树）上。这将使我能够检验几个关于促进互利依赖或其崩溃的因素的假设，我的下一个目标将是确定基因构成中的哪些变化是导致互利依赖转变的原因。到目前为止，我们对这一领域的了解仅限于与生活在宿主体内的微生物有关的互惠关系。我以前的工作已经表明，兼性互惠很容易丢失，而专性互惠是进化保守的。是什么定义了这些互惠依赖的可逆性？为了解决这些问题，我将集中讨论一种共生互惠关系，即植物寄生蚂蚁以换取额外的营养（有时还能抵御食草动物）。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，因为它们具有不同程度的依赖性。通过DNA测序，我将集中讨论三个主要问题：（1）在蚂蚁和植物的共生关系中，功能基因的缺失是否会像微生物和宿主之间的伙伴关系一样，驱动互利依赖？(2)不同程度的互惠依赖如何影响基因进化的速度？以及（3）在从兼性依赖到专性依赖的过渡过程中，我们能否识别与性状进化相关的基因组变化？最后，我将测试的假设，专性依赖于蚂蚁在这组是病原体防御功能的损失（这意味着这一功能是由蚂蚁），这是从我的初步数据产生的结果。为了做到这一点，我将在实地进行实验，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。这将反过来揭示互利依赖对微生物群落的影响。在这个项目的最后，我希望已经确定了促进互利依赖进化的条件，介导专性依赖的机制，以及它如何影响动物/植物互利共生中遗传组成的进化。由于互惠依赖影响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，义务互利主义者被认为更容易灭绝，因为他们的命运是绑定到他们的互利合作伙伴，这项研究有可能通知保护。

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.