Scaling of the risk landscape drives optimal life history strategies and the evolution of grazing

Consumers face numerous risks that can be minimized by incorporating different life-history strategies. How much and when a consumer adds to its energetic reserves or invests in reproduction are key behavioral and physiological adaptations that structure much of how organisms interact. Here we develop a theoretical framework that explicitly accounts for stochastic fluctuations of an individual consumer's energetic reserves while foraging and reproducing on a landscape with resources that range from uniformly distributed to highly clustered. First, we show that optimal life-history strategies vary in response to changes in the mean productivity of the resource landscape, where depleted environments promote reproduction at lower energetic states, greater investment in each reproduction event, and smaller litter sizes. We then show that if resource variance scales with body size due to landscape clustering, consumers that forage for clustered foods are susceptible to strong Allee effects, increasing extinction risk. Finally, we show that the proposed relationship between consumer body size, resource clustering, and Allee effect-induced population instability offers key ecological insights into the evolution of large-bodied grazing herbivores from small-bodied browsing ancestors.Comment: 9 pages, 5 figures, 3 Supplementary Appendices, 2 Supplementary Figure

Predicting Whole Forest Structure, Primary Productivity, and Biomass Density From Maximum Tree Size and Resource Limitations

In the face of uncertain biological response to climate change and the many critiques concerning model complexity it is increasingly important to develop predictive mechanistic frameworks that capture the dominant features of ecological communities and their dependencies on environmental factors. This is particularly important for critical global processes such as biomass changes, carbon export, and biogenic climate feedback. Past efforts have successfully understood a broad spectrum of plant and community traits across a range of biological diversity and body size, including tree size distributions and maximum tree height, from mechanical, hydrodynamic, and resource constraints. Recently it was shown that global scaling relationships for net primary productivity are correlated with local meteorology and the overall biomass density within a forest. Along with previous efforts, this highlights the connection between widely observed allometric relationships and predictive ecology. An emerging goal of ecological theory is to gain maximum predictive power with the least number of parameters. Here we show that the explicit dependence of such critical quantities can be systematically predicted knowing just the size of the largest tree. This is supported by data showing that forests converge to our predictions as they mature. Since maximum tree size can be calculated from local meteorology this provides a general framework for predicting the generic structure of forests from local environmental parameters thereby addressing a range of critical Earth-system questions.Comment: 26 pages, 4 figures, 1 Tabl

Metabolic scaling in small life forms

Metabolic scaling is one of the most important patterns in biology. Theory explaining the 3/4-power size-scaling of biological metabolic rate does not predict the non-linear scaling observed for smaller life forms. Here we present a new model for cells $<10^{-8}$ m$^{3}$ that maximizes power from the reaction-displacement dynamics of enzyme-catalyzed reactions. Maximum metabolic rate is achieved through an allocation of cell volume to optimize a ratio of reaction velocity to molecular movement. Small cells $< 10^{-17}$ m$^{3}$ generate power under diffusion by diluting enzyme concentration as cell volume increases. Larger cells require bulk flow of cytoplasm generated by molecular motors. These outcomes predict curves with literature-reported parameters that match the observed scaling of metabolic rates for unicells, and predicts the volume at which Prokaryotes transition to Eukaryotes. We thus reveal multiple size-dependent physical constraints for microbes in a model that extends prior work to provide a parsimonious hypothesis for how metabolism scales across small life.Comment: 22 pages, 6 figure

On the dynamics of mortality and the ephemeral nature of mammalian megafauna

Energy flow through consumer-resource interactions is largely determined by body size. Allometric relationships govern the dynamics of populations by impacting rates of reproduction, as well as alternative sources of mortality, which have differential impacts on smaller to larger organisms. Here we derive and investigate the timescales associated with four alternative sources of mortality for terrestrial mammals: mortality from starvation, mortality associated with aging, mortality from consumption by predators, and mortality introduced by anthropogenic subsidized harvest. The incorporation of these allometric relationships into a minimal consumer-resource model illuminates central constraints that may contribute to the structure of mammalian communities. Our framework reveals that while starvation largely impacts smaller-bodied species, the allometry of senescence is expected to be more difficult to observe. In contrast, external predation and subsidized harvest have greater impacts on the populations of larger-bodied species. Moreover, the inclusion of predation mortality reveals mass thresholds for mammalian herbivores, where dynamic instabilities may limit the feasibility of megafaunal populations. We show how these thresholds vary with alternative predator-prey mass relationships, which are not well understood within terrestrial systems. Finally, we use our framework to predict the harvest pressure required to induce mass-specific extinctions, which closely align with previous estimates of anthropogenic megafaunal exploitation in both paleontological and historical contexts. Together our results underscore the tenuous nature of megafaunal populations, and how different sources of mortality may contribute to their ephemeral nature over evolutionary time.Comment: 10 pages, 5 figures, 1 table, 4 appendices, 8 supplementary figure

Morphological optimization for access to dual oxidants in biofilms

A major theme driving research in biology is the relationship between form and function. In particular, a longstanding goal has been to understand how the evolution of multicellularity conferred fitness advantages. Here we show that biofilms of the bacterium Pseudomonas aeruginosa produce structures that maximize cellular reproduction. Specifically, we develop a mathematical model of resource availability and metabolic response within colony features. This analysis accurately predicts the measured distribution of two types of electron acceptors: oxygen, which is available from the atmosphere, and phenazines, redox-active antibiotics produced by the bacterium. Using this model, we demonstrate that the geometry of colony structures is optimal with respect to growth efficiency. Because our model is based on resource dynamics, we also can anticipate shifts in feature geometry based on changes to the availability of electron acceptors, including variations in the external availability of oxygen and genetic manipulation that renders the cells incapable of phenazine production

Generalized Stoichiometry and Biogeochemistry for Astrobiological Applications

A central need in the field of astrobiology is generalized perspectives on life that make it possible to differentiate abiotic and biotic chemical systems. A key component of many past and future astrobiological measurements is the elemental ratio of various samples. Classic work on Earth's oceans has shown that life displays a striking regularity in the ratio of elements as originally characterized by Redfield. The body of work since the original observations has connected this ratio with basic ecological dynamics and cell physiology, while also documenting the range of elemental ratios found in a variety of environments. Several key questions remain in considering how to best apply this knowledge to astrobiological contexts: How can the observed variation of the elemental ratios be more formally systematized using basic biological physiology and ecological or environmental dynamics? How can these elemental ratios be generalized beyond the life that we have observed on our own planet? Here we expand recently developed generalized physiological models to create a simple framework for predicting the variation of elemental ratios found in various environments. We then discuss further generalizing the physiology for astrobiological applications. Much of our theoretical treatment is designed for in situ measurements applicable to future planetary missions. We imagine scenarios where three measurements can be made - particle/cell sizes, particle/cell stoichiometry, and fluid or environmental stoichiometry - and develop our theory in connection with these often deployed measurements.Comment: 18 pages, 5 figure

Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

About 382 Tg yr⁻¹ of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia

Assembly Theory Explains and Quantifies the Emergence of Selection and Evolution

Since the time of Darwin, scientists have struggled to reconcile the evolution of biological forms in a universe determined by fixed laws. These laws underpin the origin of life, evolution, human culture and technology, as set by the boundary conditions of the universe, however these laws cannot predict the emergence of these things. By contrast evolutionary theory works in the opposite direction, indicating how selection can explain why some things exist and not others. To understand how open-ended forms can emerge in a forward-process from physics that does not include their design, a new approach to understand the non-biological to biological transition is necessary. Herein, we present a new theory, Assembly Theory (AT), which explains and quantifies the emergence of selection and evolution. In AT, the complexity of an individual observable object is measured by its Assembly Index (a), defined as the minimal number of steps needed to construct the object from basic building blocks. Combining a with the copy number defines a new quantity called Assembly which quantifies the amount of selection required to produce a given ensemble of objects. We investigate the internal structure and properties of assembly space and quantify the dynamics of undirected exploratory processes as compared to the directed processes that emerge from selection. The implementation of assembly theory allows the emergence of selection in physical systems to be quantified at any scale as the transition from undirected-discovery dynamics to a selected process within the assembly space. This yields a mechanism for the onset of selection and evolution and a formal approach to defining life. Because the assembly of an object is easily calculable and measurable it is possible to quantify a lower limit on the amount of selection and memory required to produce complexity uniquely linked to biology in the universe.Comment: 22 pages, 7 figure