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

The physical, environmental, and evolutionary determinants of biological architecture

Thesis (Ph. D. in Physical Biology)--Massachusetts Institute of Technology, Dept. of Earth, Atmospheric, and Planetary Sciences, 2013.Cataloged from PDF version of thesis.Includes bibliographical references (p. 201-224).The relationship between structure and function is a longstanding and central topic in biology, evolution, and ecology. The importance of morphology is clearly visible in the diverse forms taken by innumerable organisms in order to perform a myriad of functions. Examining the great variety of morphological characteristics it would seem that the overall principle of evolution is the only way to generalize the observed diversity: given differences in environments and random biological variation a great multitude of body plans have been invented as adaptations to many dynamic habitats given specific evolutionary histories. In this thesis I will show how focusing on diverse organisms makes it possible to identify common first-order laws of evolutionary organization. More specifically I will show how these common laws derive from a connection between organism structure, physical limitations, environmental constraints, and basic metabolic, biochemical, or energetic principles. Furthermore, I will show how this top level of biological organization holds significant predictive power for regional ecology and for interpreting the general trends of evolutionary history. In Chapter 2 we begin by deriving a model for the growth of single cells and populations of cells. This model is based on the partitioning of metabolic resources and the scaling relationship between metabolism and body size. We show that the growth of diverse classes of organisms is connected by common unit energetics. However there exist striking differences in the broad trends between growth rate and body size across these different classes and we show that this is a consequence of major evolutionary transitions which adjust the partitioning of metabolic resources. We interpret major evolutionary transitions to occur in response to energetic limitations. We also find that multicellular living for unicellular organisms provides a metabolic and reproductive advantage. In Chapters 3 and 4 we further investigate these features in microbial biofilms which exhibit rich spatial patterning. Using a mathematical model and experimentation we find that the tall vertical structures produced by these biofilms have optimal geometry for resource uptake and the growth efficiency of the entire colony. Our model allows us to predict the observed changes in feature geometry given alterations to the environmental conditions that the biofilms are grown in. Furthermore, we are able to show that the morphology of these structures is dependent on single cell physiology. For example, single genetic knockouts of flagellar motility radically alter the temporal dynamics of feature spacing. Our work highlights morphology as a central property in multicellular organisms which mediates the interaction between environmental conditions and physiology. In Chapter 5 we highlight the importance of morphology in complex multicellular life where we develop a general model of tree architecture which we link to physiological success within a given environment. Although this model is general, uses only tree size as a governing parameter, and does not consider speciation we are able use local resource availability to predict broad regional patterns in plant traits such as maximum tree height. Each of these chapters highlights the importance of structure and morphology at multiple biological scales. In Chapter 6 we show how the importance of structure extends to the genetic level where the specific encoding of a gene can have implicit information and functionality beyond the basic translation of codons. We investigate the observed implicit function of dramatic and frequent changes in the mutation rate of an organism given the structure of the mutL gene. We show mathematically that altering mutation rates is an evolutionarily advantageous strategy, and we show bioinformatically that the specific genetic structure that gives rise to this trait is under positive evolutionary selection.by Christopher Andrew Poling Kempes.Ph.D.in Physical Biolog

Epistemology and Anomaly Detection in Astrobiology

We examine the epistemological foundations of a leading technique in the search for evidence of life on exosolar planets. Specifically, we consider the ``transit method'' for spectroscopic analysis of exoplanet atmospheres, and the practice of treating anomalous chemical compositions of the atmospheres of exosolar planets as indicators of the potential presence of life. We propose a methodology for ranking the anomalousness of atmospheres that uses the mathematical apparatus of support vector machines, and which aims to be agnostic with respect to the particular chemical biosignatures of life. We argue that our approach is justified by an appeal to the "hinge" model of epistemic justification first proposed by Wittgenstein (1969). We then compare our approach to previous work due to Walker et al. (2018) and Cleland (2019a, 2019b)

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

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