The drivers of major transitions in mutualistic dependence

物种之间的合作(互惠互利)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。互惠关系从也可以在没有彼此的情况下生活的物种之间的联系(临时的)到将物种的命运捆绑在一起的紧密的义务伙伴关系。这些不同类型的互惠关系是在什么时候演变或消失的？是什么让一个物种有义务依赖另一个物种？为什么一些协会可以和平地瓦解，而在另一些情况下，离婚是死胡同？这个项目旨在了解互惠依赖是何时以及如何演变的。应对这一重大科学挑战需要在不同的尺度上分析互惠关系。我将使用三种主要方法来实现这一点。我的第一个方法将涉及绘制不同种类的动物/植物互惠关系的地图，跨越植物的生命树，以了解它们何时进化或分解。为了做到这一点，我将使用三种主要的动植物互惠作用：授粉、种子传播和植物防御草食动物或病原体。这三种生态上重要的动植物互惠关系汇聚在一起，即关键功能可以依赖于或独立于动物互惠关系。我将把这些策略映射到一个大型进化植物树(系统发育图)上。这将使我能够测试关于促进互助依赖或其崩溃的因素的几个假设。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助依赖转变的原因。到目前为止，我们对这一领域的了解仅限于与寄主体内的微生物相互作用。我之前的工作表明，兼性互惠很容易失去，而专有互惠在进化上是保守的。是什么定义了这些相互依存关系的可逆性？为了解决这些问题，我将重点介绍一种共生互惠关系，即植物寄主蚂蚁，以换取额外的营养(有时还会防御食草动物)。这组来自咖啡家族的约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，我将重点讨论三个主要问题：(1)功能基因的丧失是否会像微生物和宿主之间的伙伴关系一样，在蚂蚁和植物之间的这些共生中驱动互惠依赖？(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转变过程中，我们能否识别与性状进化相关的基因组变化？最后，我将检验这样一种假设，即对这一组蚂蚁的专性依赖是病原体防御功能丧失的结果(这意味着这一功能是由蚂蚁执行的)，这是根据我的初步数据得出的。为此，我将在田间进行实验，将蚂蚁从专性和兼性植物中移走，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。这将反过来揭示互惠依赖对微生物群落的影响。在这个项目结束时，我希望已经确定了促进互惠依赖进化的条件，专性依赖被调节的机制，以及它如何影响动植物互惠关系中基因组成的进化。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、有义务的互助者被认为更容易灭绝，因为他们的命运与他们的互惠伙伴息息相关，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.