Modelling nutritional mutualisms: challenges and opportunities for data integration

Abstract

Nutritional mutualisms are ancient, widespread, and profoundly influential in biological communities and ecosystems. Although much is known about these interactions, comprehensive answers to fundamental questions, such as how resource availability and structured interactions influence mutualism persistence, are still lacking. Mathematical modelling of nutritional mutualisms has great potential to facilitate the search for comprehensive answers to these and other fundamental questions by connecting the physiological and genomic underpinnings of mutualisms with ecological and evolutionary processes. In particular, when integrated with empirical data, models enable understanding of underlying mechanisms and generalisation of principles beyond the particulars of a given system. Here, we demonstrate how mathematical models can be integrated with data to address questions of mutualism persistence at four biological scales: cell, individual, population, and community. We highlight select studies where data has been or could be integrated with models to either inform model structure or test model predictions. We also point out opportunities to increase model rigour through tighter integration with data, and describe areas in which data is urgently needed. We focus on plant-microbe systems, for which a wealth of empirical data is available, but the principles and approaches can be generally applied to any nutritional mutualism.

Unfair trade underground revealed by integrating data with Nash bargaining models

“…Our finding of experimental support for a model of asymmetric (‘unfair’) bargaining power between M. truncatula and rhizobia vs a model of ‘fair’ trade highlights the power of integrating quantitative models with data in the study of mutualisms (Clark et al ., ), which we believe will be broadly applicable to other systems. This work improves our understanding of the drivers of quantitative variation in symbiotic nitrogen fixation, a process that makes a major contribution to the global nitrogen cycle (Fowler et al ., ) and is critical for agricultural sustainability (Herridge et al ., ).…”

“…However, it is in each partner's best interest to influence the carbon‐for‐nutrient exchange ratio (‘price’) to maximize the benefit to itself (Akçay & Roughgarden, ; Grman et al ., ), conditions that should lead to a power struggle over the price. Considerable effort has been devoted to applying economic principles to analyzing nutrient exchange, stability and other aspects of mutualisms (Weyl et al ., ; Werner et al ., ; Clark et al ., ), but there is a major gap: we do not understand how the exchange ratio and the quantity traded between plant and microbe are determined.…”

“…Increases in b correlate with increases in plant bargaining power relative to the microbial symbiont and bargaining is symmetrical when b = 0.5 (Binmore et al, 1986). Previous modeling analyses of nutrient-exchange symbioses have been limited by the absence of quantitative experimental studies in which all the major relevant parameters were measured in a single study across a range of environmental conditions and used explicitly within a mathematical framework (Clark et al, 2017). To address this knowledge gap, we measured biomass distributions, nitrogen uptake and exchange rates, photosynthetic carbon assimilation fluxes and carbon and nitrogen compositions in the model Medicago truncatulaÀEnsifer medicae (legumeÀrhizobia) symbiosis under conditions ranging from low to high nitrogen availability.…”

A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic Pedicularis species

“…Interspecific interactions have been shown to have strong effects on productivity and composition of plant communities and eventually ecosystems as a whole (Callaway et al, 2002;Larimer et al, 2014). Due to the multitrophic nature of species interactions, the direction and magnitude of these effects on plant communities are often context-specific, depending on which organisms are involved (Callaway et al, 2002;Klabi et al, 2014;Weremijewicz et al, 2018), the nature of the interactions (Larimer et al, 2014), and the abiotic environments in which the interactions occur (Pugnaire et al, 2004;Larimer et al, 2014;Clark et al, 2017). Among the interactions, those involving nutrient acquisition are fundamental for plant communities in most ecosystems (Rodr ıguez-Echeverr ıa et al, 2013;Clark et al, 2017).…”

“…Due to the multitrophic nature of species interactions, the direction and magnitude of these effects on plant communities are often context-specific, depending on which organisms are involved (Callaway et al, 2002;Klabi et al, 2014;Weremijewicz et al, 2018), the nature of the interactions (Larimer et al, 2014), and the abiotic environments in which the interactions occur (Pugnaire et al, 2004;Larimer et al, 2014;Clark et al, 2017). Among the interactions, those involving nutrient acquisition are fundamental for plant communities in most ecosystems (Rodr ıguez-Echeverr ıa et al, 2013;Clark et al, 2017). Land plants have developed different strategies to increase their capability for nutrient acquisition by associating with other species, including forming mutualistic symbioses with soil microorganisms, such as arbuscular mycorrhizal (AM) fungi for more efficient phosphorus (P) acquisition, and nitrogen-fixing bacteria for enhanced nitrogen (N) uptake (de Varennes & Goss, 2007;Smith & Smith, 2011;Castagno et al, 2014).…”