Periodic Reporting for period 4 - ELEVATE (Eco-physiological tradeoffs with crop domestication: have farming ants cracked the code?)
Periodo di rendicontazione: 2022-08-01 al 2023-01-31
The problem: Domesticated crops hardly resemble their wild ancestors, and farmers often trade higher yield in artificially optimized conditions for lower performance in fluctuating environments. Leafcutter ants (genus Atta) provide fascinating parallels with human farmers, collecting fresh vegetation fragments used as compost to produce domesticated fungal crops that feed massive societies with millions of ant orkers. However, while human agricultural systems are imperiled by rapid global changes, leafcutter ants have managed to grow a single cultivar lineage from Texas to Argentina, thriving across extreme rainfall and temperature gradients and across diverse climates over millions of years.
Importance for society: The eco-physiological mechanisms governing the leafcutter farming resiliency are poorly understood. In the ELEVATE project, I am and my team are developing integrative field and lab-based approaches to understand these mechanisms with the overarching goal of gaining these insights by unifying the study of diverse farming systems around ecological niche and evolutionary mutualism principles.
We have implemented a new in vitro 'nutrition x stress' mapping approach to visualize the fundamental and realized nutritional niche requirements of fungal cultivars. Creating multidimensional landscapes of nutrient availability (e.g. protein, carbohydrates, Na, P) and environmental stress (e.g. temperature, moisture, plant toxins, crop pathogens) we are answering three main questions:
1) What genes and biochemical pathways shape cultivar performance across interacting gradients of nutrition and stress (Objective 1)?
2) Do colonies harvest substrates to navigate nutritional contours of cultivar performance maps and avoid production tradeoffs (Objective 2)?
3) Do locally adaptive cultivar traits shape the performance of farming societies across regional ecological gradients (Objective 3), and over at least 60 million years of co-evolutionary crop domestication by farming ants (Objective 4)?
Our cutting-edge approach will deliver transformative advances to the field of eco-physiology, enabling seamless integration between field and laboratory experiments, and providing new ways to visualize evolutionary mechanisms across levels of biological organization from genes to symbiotic partnerships, and from within diverse farming assemblages to across populations spanning entire continents.
Importance for society: The eco-physiological mechanisms governing the leafcutter farming resiliency are poorly understood. In the ELEVATE project, I am and my team are developing integrative field and lab-based approaches to understand these mechanisms with the overarching goal of gaining these insights by unifying the study of diverse farming systems around ecological niche and evolutionary mutualism principles.
We have implemented a new in vitro 'nutrition x stress' mapping approach to visualize the fundamental and realized nutritional niche requirements of fungal cultivars. Creating multidimensional landscapes of nutrient availability (e.g. protein, carbohydrates, Na, P) and environmental stress (e.g. temperature, moisture, plant toxins, crop pathogens) we are answering three main questions:
1) What genes and biochemical pathways shape cultivar performance across interacting gradients of nutrition and stress (Objective 1)?
2) Do colonies harvest substrates to navigate nutritional contours of cultivar performance maps and avoid production tradeoffs (Objective 2)?
3) Do locally adaptive cultivar traits shape the performance of farming societies across regional ecological gradients (Objective 3), and over at least 60 million years of co-evolutionary crop domestication by farming ants (Objective 4)?
Our cutting-edge approach will deliver transformative advances to the field of eco-physiology, enabling seamless integration between field and laboratory experiments, and providing new ways to visualize evolutionary mechanisms across levels of biological organization from genes to symbiotic partnerships, and from within diverse farming assemblages to across populations spanning entire continents.
During the funding period, I have published 10 papers (including high-impact journals: Trends in Ecology & Evolution, Nature Ecology & Evolution, Ecology Letters, Ecology, Biology Letters, etc). Others are either in Review or In Prep. I supervised: 3 postdocs, 2 full-time scientific assistants, 9 research assistants, 14 BSc thesis students, 13 MSc thesis students, and 2 hosted PhD students. I also led 3 successful field expeditions to the Panamanian rainforest at the Smithsonian Tropical Research Institute.
The research has fostered unanticipated basic & applied research applications leading to new grants. Key technical innovations include: 1) nutritional x stress landscapes which to resolve fundamental nutritional niches, 2) fundamental and realized nutritional niches to integrate between lab and field, 3) Temperature-nutrient interactions using a modified Q10 approach, and 4) discoveries about molecular and cellular mechanisms governing nutrient transfer in symbioses. I successfully integrated planned environment stressors (micronutrients, environmental toxins, crop pathogens, abiotic gradients) into nutrition x stress landscapes.
We disseminated at international scientific meetings, through and public engagement (e.g. Kulturnatten), media coverage, and a collaboration with the Copenhagen Zoo on leafcutter ants.
WP1 focused on "the molecular mechanisms governing crop performance" and used diverse molecular methods, bioinformatics tools, advanced imaging, and in vitro experiments (e.g. transcriptomics, metabolic pathway mapping, confocal microscopy) to discover how symbionts exchange nutrients.
WP2 focused on "Eco-physiological tradeoffs with crop domestication" and integrated field experiments in Panama, DNA barcoding to identify plant fragments, NIRS analyses to identify macronutrients (protein and carbohydrates) and elemental analyses (e.g. Zn, Ca, Mn, Fe, K, etc). This work validated the niche based approaches I proposed.
WP3 focused on explaining "How farming ants grow their crops in diverse habitats" and explored cultivar stress adaptations in the lab and in the field in Panama with a focus on toxic secondary metabolites in plant fragments and variable temperatures.
WP4 addressed the question "Have farming ants cracked eco-physiological domestication tradeoffs?". I assembled an international team to use DNA barcoding and microsatellites, field mapping and monitoring of colonies, nutritional analyses, In vitro studies, laboratory feeding experiments of whole farming colonies, and phylogenetic analyses. This work revealed fundamental tradeoffs between crop yield and vulnerability with potential lessons for farming systems of humans.
The research has fostered unanticipated basic & applied research applications leading to new grants. Key technical innovations include: 1) nutritional x stress landscapes which to resolve fundamental nutritional niches, 2) fundamental and realized nutritional niches to integrate between lab and field, 3) Temperature-nutrient interactions using a modified Q10 approach, and 4) discoveries about molecular and cellular mechanisms governing nutrient transfer in symbioses. I successfully integrated planned environment stressors (micronutrients, environmental toxins, crop pathogens, abiotic gradients) into nutrition x stress landscapes.
We disseminated at international scientific meetings, through and public engagement (e.g. Kulturnatten), media coverage, and a collaboration with the Copenhagen Zoo on leafcutter ants.
WP1 focused on "the molecular mechanisms governing crop performance" and used diverse molecular methods, bioinformatics tools, advanced imaging, and in vitro experiments (e.g. transcriptomics, metabolic pathway mapping, confocal microscopy) to discover how symbionts exchange nutrients.
WP2 focused on "Eco-physiological tradeoffs with crop domestication" and integrated field experiments in Panama, DNA barcoding to identify plant fragments, NIRS analyses to identify macronutrients (protein and carbohydrates) and elemental analyses (e.g. Zn, Ca, Mn, Fe, K, etc). This work validated the niche based approaches I proposed.
WP3 focused on explaining "How farming ants grow their crops in diverse habitats" and explored cultivar stress adaptations in the lab and in the field in Panama with a focus on toxic secondary metabolites in plant fragments and variable temperatures.
WP4 addressed the question "Have farming ants cracked eco-physiological domestication tradeoffs?". I assembled an international team to use DNA barcoding and microsatellites, field mapping and monitoring of colonies, nutritional analyses, In vitro studies, laboratory feeding experiments of whole farming colonies, and phylogenetic analyses. This work revealed fundamental tradeoffs between crop yield and vulnerability with potential lessons for farming systems of humans.
This grant has enabled me to extend the field of nutritional geometry in the directions of symbioses, fungal biology, field-lab integration, and novel nutritional dimensions and scales of measurement. Each of these innovations is helping to ensure that my research group leads the field beyond the state of the art and remains competitive for funding moving forward. It's a very exciting time to study nutritional biology!
The nutrition x stress landscape (NSL) paradigm has fostered basic research advances into related systems involving fungal symbionts, including convergently evolved fungal cultivars of fungus-farming termites and insect pathogenic fungi. It has also enabled potential extensions into applied areas with possibility to solve pressing issues of insect production for food enabling potential fungal pathogens to be screened. Fine-dining restaurants have also become interested in using NSLs to find novel fungal enzymes to be used for fermentation.
The niche-based approaches has become useful for studying the ecology and evolution of other systems including other insects. For instance, a newly submitted grant explores how land use change in Denmark has changed plant communities in and thus nutritional landscapes upon which herbivorous insects forage. Another grant tries to explore nutritional landscapes at the level of individual plant metabolites.
Key advances we made in resolving the cellular mechanisms of nutrient exchange in the leafcutter ant fungal cultivar have provided a launchpad for two new fully funded grants that will allow us to continue this line of research with ever more cutting edge metabolic and nano-scale precision.
The nutrition x stress landscape (NSL) paradigm has fostered basic research advances into related systems involving fungal symbionts, including convergently evolved fungal cultivars of fungus-farming termites and insect pathogenic fungi. It has also enabled potential extensions into applied areas with possibility to solve pressing issues of insect production for food enabling potential fungal pathogens to be screened. Fine-dining restaurants have also become interested in using NSLs to find novel fungal enzymes to be used for fermentation.
The niche-based approaches has become useful for studying the ecology and evolution of other systems including other insects. For instance, a newly submitted grant explores how land use change in Denmark has changed plant communities in and thus nutritional landscapes upon which herbivorous insects forage. Another grant tries to explore nutritional landscapes at the level of individual plant metabolites.
Key advances we made in resolving the cellular mechanisms of nutrient exchange in the leafcutter ant fungal cultivar have provided a launchpad for two new fully funded grants that will allow us to continue this line of research with ever more cutting edge metabolic and nano-scale precision.