Jordan G. Okie

Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life

The diversification of life involved enormous increases in size and complexity. The evolutionary transitions from prokaryotes to unicellular eukaryotes to metazoans were accompanied by major innovations in metabolic design. Here we show that the scalings of metabolic rate, population growth rate, and production efficiency with body size have changed across the evolutionary transitions. Metabolic rate scales with body mass superlinearly in prokaryotes, linearly in protists, and sublinearly in metazoans, so Kleiber’s 3/4 power scaling law does not apply universally across organisms. The scaling of maximum population growth rate shifts from positive in prokaryotes to negative in protists and metazoans, and the efficiency of production declines across these groups. Major changes in metabolic processes during the early evolution of life overcame existing constraints, exploited new opportunities, and imposed new constraints.

Energetic Limits to Economic Growth

The human population and economy have grown exponentially and now have impacts on climate, ecosystem processes, and biodiversity far exceeding those of any other species. Like all organisms, humans are subject to natural laws and are limited by energy and other resources. In this article, we use a macro ecological approach to integrate perspectives of physics, ecology, and economics with an analysis of extensive global data to show how energy imposes fundamental constraints on economic growth and development. We demonstrate a positive scaling relationship between per capita energy use and per capita gross domestic product (GDP) both across nations and within nations over time. Other indicators of socioeconomic status and ecological impactare correlated with energy use and GDP. We estimate global energy consumption for alternative future scenarios of population growth and standards of living. Large amounts of energy will be required to fuel economic growth, increase standards of living, and lift developing nations out of poverty.

The Evolution of Maximum Body Size of Terrestrial Mammals

How Mammals Grew in Size Mammals diversified greatly after the end-Cretaceous extinction, which eliminated the dominant land animals (dinosaurs). Smith et al. (p. 1216) examined how the maximum size of mammals increased during their radiation in each continent. Overall, mammal size increased rapidly, then leveled off after about 25 million years. This pattern holds true on most of the continents—even though data are sparse for South America—and implies that mammals grew to fill available niches before other environmental and biological limits took hold. Maximum mammal size increased at the beginning of the Cenozoic, then leveled off after about 25 million years. The extinction of dinosaurs at the Cretaceous/Paleogene (K/Pg) boundary was the seminal event that opened the door for the subsequent diversification of terrestrial mammals. Our compilation of maximum body size at the ordinal level by sub-epoch shows a near-exponential increase after the K/Pg. On each continent, the maximum size of mammals leveled off after 40 million years ago and thereafter remained approximately constant. There was remarkable congruence in the rate, trajectory, and upper limit across continents, orders, and trophic guilds, despite differences in geological and climatic history, turnover of lineages, and ecological variation. Our analysis suggests that although the primary driver for the evolution of giant mammals was diversification to fill ecological niches, environmental temperature and land area may have ultimately constrained the maximum size achieved.

The Macroecology of Sustainability

Global consumption rates of vital resources suggest that we have surpassed the capacity of the Earth to sustain current levels, much less future trajectories of growth in human population and economy.

Contrasting trait responses in plant communities to experimental and geographic variation in precipitation.

• Patterns of precipitation are likely to change significantly in the coming century, with important but poorly understood consequences for plant communities. Experimental and correlative studies may provide insight into expected changes, but little research has addressed the degree of concordance between these approaches. • We synthesized results from four experimental water addition studies with a correlative analysis of community changes across a large natural precipitation gradient in the United States. We investigated whether community composition, summarized with plant functional traits, responded similarly to increasing precipitation among studies and sites. • In field experiments, increased precipitation favored species with small seed size, short leaf life span and high leaf nitrogen (N) concentration. However, with increasing precipitation along the natural gradient, community composition shifted towards species with higher mean seed mass, longer leaf life span and lower leaf N concentrations. • The differences in temporal and spatial scale of experimental manipulations and natural gradients may explain these contrasting results. Our results highlight the complexity of responses to climate change, and suggest that transient dynamics may not reflect long-term shifts in functional diversity and community composition. We propose a model of community change that incorporates these differences between short- and long-term responses to climate change.

The maximum rate of mammal evolution

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous–Paleogene (K–Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert.

ABSTRACT Microbial communities in extreme environments often have low diversity and specialized physiologies suggesting a limited resistance to change. The McMurdo Dry Valleys (MDV) are a microbially dominated, extreme ecosystem currently undergoing climate change-induced disturbances, including the melting of massive buried ice, cutting through of permafrost by streams, and warming events. These processes are increasing moisture across the landscape, altering conditions for soil communities by mobilizing nutrients and salts and stimulating autotrophic carbon inputs to soils. The goal of this study was to determine the effects of resource addition (water/organic matter) on the composition and function of microbial communities in the MDV along a natural salinity gradient representing an additional gradient of stress in an already extreme environment. Soil respiration and the activity of carbon-acquiring extracellular enzymes increased significantly (P < 0.05) with the addition of resources at the low- and moderate-salinity sites but not the high-salinity site. The bacterial community composition was altered, with an increase in Proteobacteria and Firmicutes with water and organic matter additions at the low- and moderate-salinity sites and a near dominance of Firmicutes at the high-salinity site. Principal coordinate analyses of all samples using a phylogenetically informed distance matrix (UniFrac) demonstrated discrete clustering among sites (analysis of similarity [ANOSIM], P < 0.05 and R > 0.40) and among most treatments within sites. The results from this experimental work suggest that microbial communities in this environment will undergo rapid change in response to the altered resources resulting from climate change impacts occurring in this region.

Niches, body sizes, and the disassembly of mammal communities on the Sunda Shelf islands

The rising sea level at the end of the Pleistocene that created the islands of the Sunda Shelf in Indonesia and Malaysia provides a natural experiment in community disassembly and offers insights into the effects of body size and niches on abundance, distribution, and diversity. Since isolation, terrestrial mammal communities of these islands have been reduced by extinction, with virtually no offsetting colonization. We document three empirical patterns of disassembly, all of which are significantly different from null models of random assembly: (i) a diversity–area relationship: the number of taxa is strongly and positively correlated with island area; (ii) nested subset composition: species that occur on small islands tend to be subsets of more diverse communities inhabiting larger islands; and (iii) body size distributions: species of intermediate body sizes occur on the greatest number of islands, and smaller islands have smaller ranges of body sizes, caused by the absence of species of both very large and extremely small size. These patterns reveal the role of body size and other niche characteristics, such as habitat requirements and trophic status, in the differential susceptibility of taxa to extinction.

The Malthusian-Darwinian dynamic and the trajectory of civilization.

Two interacting forces influence all populations: the Malthusian dynamic of exponential growth until resource limits are reached, and the Darwinian dynamic of innovation and adaptation to circumvent these limits through biological and/or cultural evolution. The specific manifestations of these forces in modern human society provide an important context for determining how humans can establish a sustainable relationship with the finite Earth.

General models for the spectra of surface area scaling strategies of cells and organisms: fractality, geometric dissimilitude, and internalization.

Surface areas and volumes of biological systems—from molecules to organelles, cells, and organisms—affect their biological rates and kinetics. Therefore, surface area–to-volume ratios and the scaling of surface area with volume profoundly influence ecology, physiology, and evolution. The zeroth-order geometric expectation is that surface area scales with body mass or volume as a power law with an exponent of two-thirds, with consequences for surface area–to-volume (SA∶V) ratios and constraints on size; however, organisms have adaptations for altering the surface area scaling and SA∶V ratios of their bodies and structures. The strategies fall into three groups: (1) fractal-like surface convolutions and crinkles; (2) classic geometric dissimilitude through elongating, flattening, fattening, and hollowing; and (3) internalization of surfaces. Here I develop general quantitative theory to model the spectra of effects of these strategies on SA∶V ratios and surface area scaling, from exponents of less than two-thirds to superlinear scaling and mixed-power laws. Applying the theory to cells helps quantitatively evaluate the effects of membrane fractality, shape-shifting, vacuoles, vesicles, and mitochondria on surface area scaling, informing understanding of cell allometry, morphology, and evolution. Analysis of compiled data indicates that through hollowness and surface internalization, eukaryotic phytoplankton increase their effective surface area scaling, attaining near-linear scaling in larger cells. This unifying theory highlights the fundamental role of biological surfaces in metabolism and morphological evolution.