The drivers of major transitions in mutualistic dependence

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.

Who could potentially benefit from the proposed research over different timescales?

I will address a fundamental evolutionary question on ecological interactions, which will benefit academics from various disciplines (see Academic beneficiaries). To address this question, I use animal/plant mutualisms. These charismatic associations fuelled a lot of interest in the general public. Moreover, since mutualism dependence binds species together, it can affect extinction risks and therefore this research can be beneficial to conservation at different levels.

How might the potential beneficiaries benefit?

General public: I will disseminate my research widely to the general public. Pitching fundamental evolutionary questions to the general public can be difficult due to the lack of interest in classical study systems. My discovery of the first true agriculture involving ants that plant and fertilize their host plant as well as cultivate, defend, and fertilize seedlings of their epiphyte has fuelled massive interest from the global public. This agriculture evolved long before that of humans and thus has a wide audience besides biologists. My recent paper in Nature Plants, which describes this Fijian ant/plant farming mutualism, was featured in more than 100 medias in over 15 languages (http://www.nature.com/articles/nplants2016181/metrics), including Nature, Science, The Economist, or New Scientist and led to several radio interviews (BBC World News, CBS, Radio Australia and Deutschlandfunk). I will use this high public interest in my research system to empower public science communication.
This attractiveness of the public to my research theme is ideal because it allows me to introduce several biological themes in an entertaining and exciting way across a wide range of topics not only in evolution and ecology, but also in conservation by pinpointing how being dependent on other organisms can increase extinction risk if these other organisms become threatened. The attractiveness of animal/plant mutualisms and the visual impact they have will help in designing science communication schemes for three main groups of beneficiaries from the general public: (i) children, to whom ideas about both evolution and conservation can be communicated through visual (including video) media using animal/plant mutualisms; (ii) all-age general public and (iii) Fijian children, whose interest can have direct impact for conservation locally. The pathway to impact section details how I will engage with these groups.

Conservation: The proposed research benefits conservation at different levels. By binding species fate together, obligate dependence can increase extinction risks. In these Fijian ant/plant symbioses, my research indeed suggests small ranges and highly vulnerable conservation status, with one species likely on the verge of extinction. A conservation plan for those species will directly impact their conservation, and that of hundreds of other species living in these Fijian rainforests. Details regarding the implementation of this conservation plan is provided in the Pathway to impact.
Second, the charismatic nature of these Fijian ant/plant symbioses, together with their attractiveness to the general public, could lead to the development of flagship species.
Finally, the maps of mutualism dependencies could inform conservation by pinpointing hotspots where communities are highly dependent on other organisms, and thus more vulnerable.