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REciprocal LOcal ADapatation: the genetic, behavioural and chemical study of the evolutionary maintenance of a mutualism

Periodic Reporting for period 1 - RELOAD (REciprocal LOcal ADapatation: the genetic, behavioural and chemical study of the evolutionary maintenance of a mutualism)

Reporting period: 2016-07-01 to 2018-06-30

Devil’s Gardens are clearings in the Amazonian rainforest where only the treelet Duroia hirsuta can grow. According to local folklore, these orchard-like stands are created by a forest spirit, hence their name. They are actually cultivated by the arboreal ants Myrmelachista schumanni, whose workers systematically attack and kill seedlings of foreign plants that germinate too close to their host plants. This cultivation behaviour results in monocultures of D. hirsuta in the middle of some of the most diverse rainforests on earth. Devil’s Gardens are one of the very few examples of non-human agriculture.
The goal of this project is to identify and characterize genetic, behavioural and biochemical mechanisms involved in this fascinating ant-plant relationship. The main questions addressed are: (1) does the geographical organization in Devil’s Gardens influence D. hirsuta and M. schumanni genetic diversity? (2) How specialized are interactions between M. schumanni and its host-plant? (3) What is the impact of Devil’s Gardens on environmental diversity?
This project holds potential for tremendous scholarly impact in the field of mutualism study, and for tangible socio-economic impact in agriculture. Mutualism stability in face of cheating is one of the hot research topics of the decade in biology. This project will provide invaluable information about genetic diversity underlying the functioning of one of the most fascinating model systems of specialized mutualisms. On the other hand, Devil’s Gardens face the same issues as human agriculture: increased herbivore and pathogen pressures. Learning how ants have been circumventing these issues for the past million years can inform human practices and provide solutions for a more sustainable agriculture.
Objective 1: characterizing the population genetic structure of both partners
I collected several hundred samples of M. schumanni and D. hirsuta across the Western Amazon rainforest. I developed tailor-made molecular biology protocols to isolate their DNA and RNA, and analyse them. I finally sequenced their genomes using cutting-edge technologies that were previously not available for non-model species. I am currently in the process of analysing the population genetic data in the light of the genome assemblies.

Objective 2: assessment of the specialisation of ants to their host-plants
I collected thousands of seeds across Peru, planted hundreds of them, and finally grew more than 100 seedlings of D. hirsuta. I took care of them in a common garden in the rainforest, protected them from herbivores and ants. After one year, I transplanted these seedlings to three naturally occurring Devil’s Gardens and observed the ant behaviour. Interestingly, the ants did not attack the newcomers and tolerated them all, whether the seeds were coming from a local plant or a very distant one. Therefore, the degree of specialisation of the association does not encompass the intraspecific level.

Objective 3: assessment of the impact of Devil’s Gardens on local diversity
I measured the germination success of four plant species under different conditions involving soil from Devil’s Gardens. The results indicate that D. hirsuta prevents seed germination and mould development through modifications of soil chemistry.
This project already unveiled crucial details about non-human agriculture, about ant-plant mutualisms, and particularly about the natural history of Devil’s Gardens. We learned that the adaptation of ants to their host is loose enough for them to accept any host-plant from the right species. These results dismiss the hypothesis of strong genetic associations between species. We also learned that both ants and plants modify Devil’s Garden environment to get rid of plant competitors and to increase protection against fungal parasites.
All the experiments started during the first phase of the project are about to come to fruition over the next weeks. The expected results will shed light on the evolutionary history of Devil’s Gardens, they will allow for the identification of the mechanisms underlying soil modification by D. hirsuta, and they will establish the consequences of environment modification for microbe biodiversity.
So far, the project led to new collaborations between laboratories in the USA, Peru, Ecuador, and Germany. I mentored three undergrad students, organised three field expeditions to the jungle for myself and other researchers, and successfully applied for additional funding for the project, thus gaining valuable experience in people and project management. Daily progress of the project is being popularised on social media, in particular through original short films.
Myrmelachista schumanni ants patroling on a domatium of Duroia hirsuta, their host plant.