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INSEAME Report Summary

Project ID: 327940
Funded under: FP7-PEOPLE
Country: Denmark

Final Report Summary - INSEAME (INtegrating Social Evolution and Metabolic Ecology)

The central aim of this project was to understand the physiological basis of major transitions in the evolution and ecology of ant societies, using fungus-growing attine ants as a model system. I used an integrative physiological framework to examine the nutritional consequences of crop domestication by these farming ant societies. This research, performed in collaboration with scientists from the Smithsonian Tropical Research Institute (STRI) and the University of Copenhagen proceeded according to schedule. I also fulfilled the transfer of knowledge objectives by organizing and teaching an international field course titled “Tropical Behavioral Ecology and Evolution” at STRI in 2011, 2013, and 2015. This led to extended mentorship beyond the course period and published papers. I also established an advanced insect physiology laboratory at the University of Copenhagen that has fostered numerous collaborations.

I had successful field seasons at STRI in Panama during the summers of 2014 and 2015. During the field season lasting from May-June in 2015, I used innovative ‘artificial insemination’ techniques to test whether metabolic costs of sperm storage increase with the number of stored sperm and higher mating frequency, and also tested whether nutritional choices mediate cooperation and conflict between fungus growing ants and their social parasites (unrelated ants that live in their fungus gardens). I also initiated a comparative follow-up study building on techniques I established during year 1 to map physiological requirements of attine fungal cultivars across >50 million years of evolutionary history. This involved collaborating with a Panamanian intern from August 2015 to March 2016. We are currently analyzing over 9,000 petri dishes where fungal cultivars from 11 attine species have been grown on various nutritional media. Beginning in September 2015, I also began supervising a Danish Masters student on research in Panama and Copenhagen based on my Marie Curie Funded Research. My research progress closely followed the timetable specified in Annex 1 of the Grant Agreement. I expanded the proposed hypotheses according to preliminary data collected in the year prior to the funding period specified by the Marie Curie Fellowship. Specifically, I performed a series of experiments focused on testing nutritional (rather than purely energetic) hypotheses by developing an innovative microbiological approach to explore the resource requirements of not just ant farmers, but also their fungal cultivars. This research continued throughout the funding period in Panama and in Copenhagen as specified by the proposed research timeline.

The first major paper to emerge from this research, which I performed in collaboration with scientists from the US, Britain, Denmark, and Panama, is currently in review (pending resubmission after receiving very positive initial reviews) at a top scientific journal, Proceedings of the National Academy of Sciences, USA. Its findings show parallels with early Neolithic human subsistence farmers that faced significant physiological challenges until they genetically isolated their crops through artificial selection and polyploidization. Specifically, the attine ants faced analogous challenges when they adopted fungus farming 50 MYA. While evolutionarily derived attine lineages irreversibly domesticated cultivars 20 MYA and ultimately realized industrial-scale farming, basal lineages retained small-scale farming, diversified, and now coexist with advanced fungus-farmers in most (sub)tropical ecosystems. We show that management of independent sexual reproduction in cultivars constrained farming productivity echoing early human farming of unspecialized, low-productivity crops. Loss of cultivar gene exchange with non-domesticated relatives likely reduced host-symbiont conflict over reproduction, fostering the rise of ecologically dominant ant-agriculture and broadening our understanding of the general principles by which farming practices evolve. To date, I have published 4 papers during the funding period in the following international journals: The American Naturalist, Animal Behaviour (2 papers), Journal of Evolutionary Biology. I additionally currently have a paper in review at Insectes Sociaux written with a collaborator from the University of Hong Kong. Several additional papers are also close to submission (Biology Letters and Functional Ecology) related to these findings. A series of additional exciting collaborations with European postgraduate students, Panamanian researchers and scientists at the University of Copenhagen have also unfolded. One of these projects, collaboration with a scientist from Kew Gardens (Britain) and University of Loja (Ecuador) involves an extensive molecular barcoding project designed to explore the ecological diversification of farming practices in a diverse Panamanian fungus-growing ant community. I additionally recently published a paper (Rytter and Shik 2016, Animal Behaviour) stemming from my Marie Curie funded research with a Danish Masters student that I have supervised during my stay in Europe. She is planning to pursue a PhD building on the graduate-level research we developed together.

Key innovations arising from my research involve expanding existing physiological approaches in novel ways for the study of symbiotic partnerships in order to show how ant farmers use nutrition to navigate production tradeoffs with fungal crops that often have divergent evolutionary interests. I have capitalized on the fact that despite fascinating parallels with human farming systems, ant agricultural symbioses evolved by natural selection only, allowing formulation of domestication dynamics using general evolutionary theory about host-symbiont conflict. With this approach, I have been able to demonstrate fundamental farming constraints stemming from incomplete domestication in the form of decision dilemmas with collateral damage akin to killing beneficial cells along with cancerous cells during chemotherapy, or eradicating useful insects when applying pesticides. These conclusions are based on a novel approach combining extensive field surveys, molecular data, and integrative nutritional experiments under controlled conditions. This work will thus be of interest to a substantial community of biologists, anthropologists and agricultural professionals, as well as the interested lay public.

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