Since the modern evolutionary synthesis was first proposed early in the twentieth century, attent... more Since the modern evolutionary synthesis was first proposed early in the twentieth century, attention has focused on assessing the relative contribution of mutation versus natural selection on protein evolution. Here we test a model that yields general quantitative predictions on rates of protein evolution by combining principles of individual energetics with Kimura's neutral theory. The model successfully predicts much of the heterogeneity in rates of protein evolution for diverse eukaryotes (i.e. fishes, amphibians, reptiles, birds, mammals) from different thermal environments. Data also show that the ratio of non-synonymous to synonymous nucleotide substitution is independent of body size, and thus presumably of effective population size. These findings indicate that rates of protein evolution are largely controlled by mutation rates, which in turn are strongly influenced by individual metabolic rate.
ABSTRACT The aggregation of individuals into colonies raises important questions about scaling of... more ABSTRACT The aggregation of individuals into colonies raises important questions about scaling of structure and function. We model the metabolic benefits and costs of two-dimensional, fractallike foraging trails, such as those used by ant colonies. Total area foraged by the colony and, consequently, resource flow to the nest and rate of colony metabolism, increase non-linearly with number of foragers (F) as F 2/3.
10 indicates that Pathfinder rocks may have a high water content, which supports a non-igneous cl... more 10 indicates that Pathfinder rocks may have a high water content, which supports a non-igneous classification. Formation mechanisms on a global scale are required to explain the extensive distrib- ution of type-2 materials in the northern lowlands. The weathered-basalt interpreta- tion would predict a large body of water or sedimentary depocentre in the northern lowlands, but does not account for
Understanding energy and material fluxes through ecosystems is central to many questions in globa... more Understanding energy and material fluxes through ecosystems is central to many questions in global change biology and ecology. Ecosystem respiration is a critical component of the carbon cycle and might be important in regulating biosphere response to global climate change. Here we derive a general model of ecosystem respiration based on the kinetics of metabolic reactions and the scaling of
The tremendous variation in brain size among vertebrates has long been thought to be related to d... more The tremendous variation in brain size among vertebrates has long been thought to be related to differences in species' metabolic rates. It is thought that species with higher metabolic rates can supply more energy to support the relatively high cost of brain tissue. And yet, while body temperature is known to be a major determinant of metabolic rate, the possible effects of temperature on brain size have scarcely been explored. Thus, here we explore the effects of temperature on brain size among diverse vertebrates (fishes, amphibians, reptiles, birds and mammals). We find that, after controlling for body size, brain size increases exponentially with temperature in much the same way as metabolic rate. These results suggest that temperaturedependent changes in aerobic capacity, which have long been known to affect physical performance, similarly affect brain size. The observed temperature-dependence of brain size may explain observed gradients in brain size among both ectotherms and endotherms across broad spatial and temporal scales. How to cite this article Gillooly and McCoy (2014), Brain size varies with temperature in vertebrates. PeerJ 2:e301; Krogh A. 1916. The respiratory exchange of animals and man. London: Longmans Green. Macphail E. 1982. Brain and intelligence in vertebrates. Oxford: Clarendon Press. Martin R. 1981. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature Sol D, Price T. 2008. Brain size and the diversification of body size in birds.
Aerobic activity levels increase with body temperature across vertebrates. Differences in these l... more Aerobic activity levels increase with body temperature across vertebrates. Differences in these levels, from highly active to sedentary, are reflected in their ecology and behavior. Yet, the changes in the cardiovascular system that allow for greater oxygen supply at higher temperatures, and thus greater aerobic activity, remain unclear. Here we show that the total volume of red blood cells in the body increases exponentially with temperature across vertebrates, after controlling for effects of body size and taxonomy. These changes are accompanied by increases in relative heart mass, an indicator of aerobic activity. The results point to one way vertebrates may increase oxygen supply to meet the demands of greater activity at higher temperatures.
Background: A better understanding of the size and abundance of open reading frames (ORFS) in who... more Background: A better understanding of the size and abundance of open reading frames (ORFS) in whole genomes may shed light on the factors that control genome complexity. Here we examine the statistical distributions of open reading frames (i.e. distribution of start and stop codons) in the fully sequenced genomes of 297 prokaryotes, and 14 eukaryotes.
The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prom... more The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prominent but least understood features of life on Earth. Here we show that species diversity can be predicted from the biochemical kinetics of metabolism. We first demonstrate that the average energy flux of populations is temperature invariant. We then derive a model that quantitatively predicts how species diversity increases with environmental temperature. Predictions are supported by data for terrestrial, freshwater, and marine taxa along latitudinal and elevational gradients. These results establish a thermodynamic basis for the regulation of species diversity and the organization of ecological communities.
We derive a general model, based on principles of biochemical kinetics and allometry, that charac... more We derive a general model, based on principles of biochemical kinetics and allometry, that characterizes the effects of temperature and body mass on metabolic rate. The model fits metabolic rates of microbes, ectotherms, endotherms (including those in hibernation), and plants in temperatures ranging from 0 degrees to 40 degrees C. Mass- and temperature-compensated resting metabolic rates of all organisms are similar: The lowest (for unicellular organisms and plants) is separated from the highest (for endothermic vertebrates) by a factor of about 20. Temperature and body size are primary determinants of biological time and ecological roles.
Proceedings of the National Academy of Sciences, 2006
Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly und... more Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly understood. We derive a model that quantifies the role of kinetic energy in generating biodiversity. The model predicts that rates of genetic divergence and speciation are both governed by metabolic rate and therefore show the same exponential temperature dependence (activation energy of Ϸ0.65 eV; 1 eV ؍ 1.602 ؋ 10 ؊19 J). Predictions are supported by global datasets from planktonic foraminifera for rates of DNA evolution and speciation spanning 30 million years. As predicted by the model, rates of speciation increase toward the tropics even after controlling for the greater ocean coverage at tropical latitudes. Our model and results indicate that individual metabolic rate is a primary determinant of evolutionary rates: Ϸ10 13 J of energy flux per gram of tissue generates one substitution per nucleotide in the nuclear genome, and Ϸ10 23 J of energy flux per population generates a new species of foraminifera. allopatric speciation ͉ biodiversity ͉ macroevolution ͉ metabolic theory of ecology ͉ molecular clock T he latitudinal increase in biodiversity from the poles to the equator is the most pervasive feature of biogeography. For two centuries, since the time of von Humboldt, Darwin, and Wallace, scientists have proposed hypotheses to explain this pattern. New species arise through the evolution of genetic differences among populations from a common ancestral lineage (1-4). Many hypotheses therefore attribute the latitudinal biodiversity gradient to a gradient in speciation rates caused by some independent variable, such as earth surface area or solar energy input (5-7). Some fossil data suggest that speciation rates do indeed increase toward the tropics (8-10), but these findings remain open to debate due in part to our limited understanding of the factors that control macroevolutionary dynamics.
Proceedings of the National Academy of Sciences, 2007
The size and metabolic rate of cells affect processes from the molecular to the organismal level.... more The size and metabolic rate of cells affect processes from the molecular to the organismal level. We present a quantitative, theoretical framework for studying relationships among cell volume, cellular metabolic rate, body size, and whole-organism metabolic rate that helps reveal the feedback between these levels of organization. We use this framework to show that average cell volume and average cellular metabolic rate cannot both remain constant with changes in body size because of the well known body-size dependence of whole-organism metabolic rate. Based on empirical data compiled for 18 cell types in mammals, we find that many cell types, including erythrocytes, hepatocytes, fibroblasts, and epithelial cells, follow a strategy in which cellular metabolic rate is body size dependent and cell volume is body size invariant. We suggest that this scaling holds for all quickly dividing cells, and conversely, that slowly dividing cells are expected to follow a strategy in which cell volume is body size dependent and cellular metabolic rate is roughly invariant with body size. Data for slowly dividing neurons and adipocytes show that cell volume does indeed scale with body size. From these results, we argue that the particular strategy followed depends on the structural and functional properties of the cell type. We also discuss consequences of these two strategies for cell number and capillary densities. Our results and conceptual framework emphasize fundamental constraints that link the structure and function of cells to that of whole organisms.
Proceedings of the National Academy of Sciences, 2005
Observations that rates of molecular evolution vary widely within and among lineages have cast do... more Observations that rates of molecular evolution vary widely within and among lineages have cast doubts on the existence of a single ''molecular clock.'' Differences in the timing of evolutionary events estimated from genetic and fossil evidence have raised further questions about the accuracy of molecular clocks. Here, we present a model of nucleotide substitution that combines theory on metabolic rate with the now-classic neutral theory of molecular evolution. The model quantitatively predicts rate heterogeneity and may reconcile differences in molecular-and fossil-estimated dates of evolutionary events. Model predictions are supported by extensive data from mitochondrial and nuclear genomes. By accounting for the effects of body size and temperature on metabolic rate, this model explains heterogeneity in rates of nucleotide substitution in different genes, taxa, and thermal environments. This model also suggests that there is indeed a single molecular clock, as originally proposed by Zuckerkandl and Pauling [Zuckerkandl, E. & Pauling, L. (1965) in Evolving Genes and Proteins, eds. Bryson, V. & Vogel, H. J. (Academic, New York), pp. 97-166], but that it ''ticks'' at a constant substitution rate per unit of mass-specific metabolic energy rather than per unit of time. This model therefore links energy flux and genetic change. More generally, the model suggests that body size and temperature combine to control the overall rate of evolution through their effects on metabolism.
Body size and temperature are the two most important variables affecting nearly all biological ra... more Body size and temperature are the two most important variables affecting nearly all biological rates and times. The relationship of size and temperature to development is of particular interest, because during ontogeny size changes and temperature often varies. Here we derive a general model, based on first principles of allometry and biochemical kinetics, that predicts the time of ontogenetic development as a function of body mass and temperature. The model fits embryonic development times spanning a wide range of egg sizes and incubation temperatures for birds and aquatic ectotherms (fish, amphibians, aquatic insects and zooplankton). The model also describes nearly 75% of the variation in post-embryonic development among a diverse sample of zooplankton. The remaining variation is partially explained by stoichiometry, specifically the whole-body carbon to phosphorus ratio. Development in other animals at other life stages is also described by this model. These results suggest a general definition of biological time that is approximately invariant and common to all organisms.
Understanding energy and material fluxes through ecosystems is central to many questions in globa... more Understanding energy and material fluxes through ecosystems is central to many questions in global change biology and ecology . Ecosystem respiration is a critical component of the carbon cycle 1,5-7 and might be important in regulating biosphere response to global climate change 1-3 . Here we derive a general model of ecosystem respiration based on the kinetics of metabolic reactions 11-13 and the scaling of resource use by individual organisms . The model predicts that fluxes of CO 2 and energy are invariant of ecosystem biomass, but are strongly influenced by temperature, variation in cellular metabolism and rates of supply of limiting resources (water and/or nutrients). Variation in ecosystem respiration within sites, as calculated from a network of CO 2 flux towers 5,7 , provides robust support for the model's predictions. However, data indicate that variation in annual flux between sites is not strongly dependent on average site temperature or latitude. This presents an interesting paradox with regard to the expected temperature dependence. Nevertheless, our model provides a basis for quantitatively understanding energy and material flux between the atmosphere and biosphere.
Analysis of zooplankton communities in over 1,100 water bodies spanning the Western Hemisphere (7... more Analysis of zooplankton communities in over 1,100 water bodies spanning the Western Hemisphere (778S, 818N latitude) revealed latitudinal patterns in cladoceran body size and Daphnia seasonal dynamics. The mean body length of cladoceran species occurring at different latitudinal intervals was greatest in north temperate regions, declining in size toward the poles and equator. Thus, mean cladoceran size was greatest in
... JF Gillooly and SI Dodson Department of Zoology, 430 Lincoln Drive, University of Wisconsin, ... more ... JF Gillooly and SI Dodson Department of Zoology, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA (Accepted 18 August 1999) ... We also thank Matthew Brewer, Bill Karasov, and Chris Tracy for critically reading the manuscript. ...
Since the modern evolutionary synthesis was first proposed early in the twentieth century, attent... more Since the modern evolutionary synthesis was first proposed early in the twentieth century, attention has focused on assessing the relative contribution of mutation versus natural selection on protein evolution. Here we test a model that yields general quantitative predictions on rates of protein evolution by combining principles of individual energetics with Kimura's neutral theory. The model successfully predicts much of the heterogeneity in rates of protein evolution for diverse eukaryotes (i.e. fishes, amphibians, reptiles, birds, mammals) from different thermal environments. Data also show that the ratio of non-synonymous to synonymous nucleotide substitution is independent of body size, and thus presumably of effective population size. These findings indicate that rates of protein evolution are largely controlled by mutation rates, which in turn are strongly influenced by individual metabolic rate.
ABSTRACT The aggregation of individuals into colonies raises important questions about scaling of... more ABSTRACT The aggregation of individuals into colonies raises important questions about scaling of structure and function. We model the metabolic benefits and costs of two-dimensional, fractallike foraging trails, such as those used by ant colonies. Total area foraged by the colony and, consequently, resource flow to the nest and rate of colony metabolism, increase non-linearly with number of foragers (F) as F 2/3.
10 indicates that Pathfinder rocks may have a high water content, which supports a non-igneous cl... more 10 indicates that Pathfinder rocks may have a high water content, which supports a non-igneous classification. Formation mechanisms on a global scale are required to explain the extensive distrib- ution of type-2 materials in the northern lowlands. The weathered-basalt interpreta- tion would predict a large body of water or sedimentary depocentre in the northern lowlands, but does not account for
Understanding energy and material fluxes through ecosystems is central to many questions in globa... more Understanding energy and material fluxes through ecosystems is central to many questions in global change biology and ecology. Ecosystem respiration is a critical component of the carbon cycle and might be important in regulating biosphere response to global climate change. Here we derive a general model of ecosystem respiration based on the kinetics of metabolic reactions and the scaling of
The tremendous variation in brain size among vertebrates has long been thought to be related to d... more The tremendous variation in brain size among vertebrates has long been thought to be related to differences in species' metabolic rates. It is thought that species with higher metabolic rates can supply more energy to support the relatively high cost of brain tissue. And yet, while body temperature is known to be a major determinant of metabolic rate, the possible effects of temperature on brain size have scarcely been explored. Thus, here we explore the effects of temperature on brain size among diverse vertebrates (fishes, amphibians, reptiles, birds and mammals). We find that, after controlling for body size, brain size increases exponentially with temperature in much the same way as metabolic rate. These results suggest that temperaturedependent changes in aerobic capacity, which have long been known to affect physical performance, similarly affect brain size. The observed temperature-dependence of brain size may explain observed gradients in brain size among both ectotherms and endotherms across broad spatial and temporal scales. How to cite this article Gillooly and McCoy (2014), Brain size varies with temperature in vertebrates. PeerJ 2:e301; Krogh A. 1916. The respiratory exchange of animals and man. London: Longmans Green. Macphail E. 1982. Brain and intelligence in vertebrates. Oxford: Clarendon Press. Martin R. 1981. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature Sol D, Price T. 2008. Brain size and the diversification of body size in birds.
Aerobic activity levels increase with body temperature across vertebrates. Differences in these l... more Aerobic activity levels increase with body temperature across vertebrates. Differences in these levels, from highly active to sedentary, are reflected in their ecology and behavior. Yet, the changes in the cardiovascular system that allow for greater oxygen supply at higher temperatures, and thus greater aerobic activity, remain unclear. Here we show that the total volume of red blood cells in the body increases exponentially with temperature across vertebrates, after controlling for effects of body size and taxonomy. These changes are accompanied by increases in relative heart mass, an indicator of aerobic activity. The results point to one way vertebrates may increase oxygen supply to meet the demands of greater activity at higher temperatures.
Background: A better understanding of the size and abundance of open reading frames (ORFS) in who... more Background: A better understanding of the size and abundance of open reading frames (ORFS) in whole genomes may shed light on the factors that control genome complexity. Here we examine the statistical distributions of open reading frames (i.e. distribution of start and stop codons) in the fully sequenced genomes of 297 prokaryotes, and 14 eukaryotes.
The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prom... more The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prominent but least understood features of life on Earth. Here we show that species diversity can be predicted from the biochemical kinetics of metabolism. We first demonstrate that the average energy flux of populations is temperature invariant. We then derive a model that quantitatively predicts how species diversity increases with environmental temperature. Predictions are supported by data for terrestrial, freshwater, and marine taxa along latitudinal and elevational gradients. These results establish a thermodynamic basis for the regulation of species diversity and the organization of ecological communities.
We derive a general model, based on principles of biochemical kinetics and allometry, that charac... more We derive a general model, based on principles of biochemical kinetics and allometry, that characterizes the effects of temperature and body mass on metabolic rate. The model fits metabolic rates of microbes, ectotherms, endotherms (including those in hibernation), and plants in temperatures ranging from 0 degrees to 40 degrees C. Mass- and temperature-compensated resting metabolic rates of all organisms are similar: The lowest (for unicellular organisms and plants) is separated from the highest (for endothermic vertebrates) by a factor of about 20. Temperature and body size are primary determinants of biological time and ecological roles.
Proceedings of the National Academy of Sciences, 2006
Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly und... more Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly understood. We derive a model that quantifies the role of kinetic energy in generating biodiversity. The model predicts that rates of genetic divergence and speciation are both governed by metabolic rate and therefore show the same exponential temperature dependence (activation energy of Ϸ0.65 eV; 1 eV ؍ 1.602 ؋ 10 ؊19 J). Predictions are supported by global datasets from planktonic foraminifera for rates of DNA evolution and speciation spanning 30 million years. As predicted by the model, rates of speciation increase toward the tropics even after controlling for the greater ocean coverage at tropical latitudes. Our model and results indicate that individual metabolic rate is a primary determinant of evolutionary rates: Ϸ10 13 J of energy flux per gram of tissue generates one substitution per nucleotide in the nuclear genome, and Ϸ10 23 J of energy flux per population generates a new species of foraminifera. allopatric speciation ͉ biodiversity ͉ macroevolution ͉ metabolic theory of ecology ͉ molecular clock T he latitudinal increase in biodiversity from the poles to the equator is the most pervasive feature of biogeography. For two centuries, since the time of von Humboldt, Darwin, and Wallace, scientists have proposed hypotheses to explain this pattern. New species arise through the evolution of genetic differences among populations from a common ancestral lineage (1-4). Many hypotheses therefore attribute the latitudinal biodiversity gradient to a gradient in speciation rates caused by some independent variable, such as earth surface area or solar energy input (5-7). Some fossil data suggest that speciation rates do indeed increase toward the tropics (8-10), but these findings remain open to debate due in part to our limited understanding of the factors that control macroevolutionary dynamics.
Proceedings of the National Academy of Sciences, 2007
The size and metabolic rate of cells affect processes from the molecular to the organismal level.... more The size and metabolic rate of cells affect processes from the molecular to the organismal level. We present a quantitative, theoretical framework for studying relationships among cell volume, cellular metabolic rate, body size, and whole-organism metabolic rate that helps reveal the feedback between these levels of organization. We use this framework to show that average cell volume and average cellular metabolic rate cannot both remain constant with changes in body size because of the well known body-size dependence of whole-organism metabolic rate. Based on empirical data compiled for 18 cell types in mammals, we find that many cell types, including erythrocytes, hepatocytes, fibroblasts, and epithelial cells, follow a strategy in which cellular metabolic rate is body size dependent and cell volume is body size invariant. We suggest that this scaling holds for all quickly dividing cells, and conversely, that slowly dividing cells are expected to follow a strategy in which cell volume is body size dependent and cellular metabolic rate is roughly invariant with body size. Data for slowly dividing neurons and adipocytes show that cell volume does indeed scale with body size. From these results, we argue that the particular strategy followed depends on the structural and functional properties of the cell type. We also discuss consequences of these two strategies for cell number and capillary densities. Our results and conceptual framework emphasize fundamental constraints that link the structure and function of cells to that of whole organisms.
Proceedings of the National Academy of Sciences, 2005
Observations that rates of molecular evolution vary widely within and among lineages have cast do... more Observations that rates of molecular evolution vary widely within and among lineages have cast doubts on the existence of a single ''molecular clock.'' Differences in the timing of evolutionary events estimated from genetic and fossil evidence have raised further questions about the accuracy of molecular clocks. Here, we present a model of nucleotide substitution that combines theory on metabolic rate with the now-classic neutral theory of molecular evolution. The model quantitatively predicts rate heterogeneity and may reconcile differences in molecular-and fossil-estimated dates of evolutionary events. Model predictions are supported by extensive data from mitochondrial and nuclear genomes. By accounting for the effects of body size and temperature on metabolic rate, this model explains heterogeneity in rates of nucleotide substitution in different genes, taxa, and thermal environments. This model also suggests that there is indeed a single molecular clock, as originally proposed by Zuckerkandl and Pauling [Zuckerkandl, E. & Pauling, L. (1965) in Evolving Genes and Proteins, eds. Bryson, V. & Vogel, H. J. (Academic, New York), pp. 97-166], but that it ''ticks'' at a constant substitution rate per unit of mass-specific metabolic energy rather than per unit of time. This model therefore links energy flux and genetic change. More generally, the model suggests that body size and temperature combine to control the overall rate of evolution through their effects on metabolism.
Body size and temperature are the two most important variables affecting nearly all biological ra... more Body size and temperature are the two most important variables affecting nearly all biological rates and times. The relationship of size and temperature to development is of particular interest, because during ontogeny size changes and temperature often varies. Here we derive a general model, based on first principles of allometry and biochemical kinetics, that predicts the time of ontogenetic development as a function of body mass and temperature. The model fits embryonic development times spanning a wide range of egg sizes and incubation temperatures for birds and aquatic ectotherms (fish, amphibians, aquatic insects and zooplankton). The model also describes nearly 75% of the variation in post-embryonic development among a diverse sample of zooplankton. The remaining variation is partially explained by stoichiometry, specifically the whole-body carbon to phosphorus ratio. Development in other animals at other life stages is also described by this model. These results suggest a general definition of biological time that is approximately invariant and common to all organisms.
Understanding energy and material fluxes through ecosystems is central to many questions in globa... more Understanding energy and material fluxes through ecosystems is central to many questions in global change biology and ecology . Ecosystem respiration is a critical component of the carbon cycle 1,5-7 and might be important in regulating biosphere response to global climate change 1-3 . Here we derive a general model of ecosystem respiration based on the kinetics of metabolic reactions 11-13 and the scaling of resource use by individual organisms . The model predicts that fluxes of CO 2 and energy are invariant of ecosystem biomass, but are strongly influenced by temperature, variation in cellular metabolism and rates of supply of limiting resources (water and/or nutrients). Variation in ecosystem respiration within sites, as calculated from a network of CO 2 flux towers 5,7 , provides robust support for the model's predictions. However, data indicate that variation in annual flux between sites is not strongly dependent on average site temperature or latitude. This presents an interesting paradox with regard to the expected temperature dependence. Nevertheless, our model provides a basis for quantitatively understanding energy and material flux between the atmosphere and biosphere.
Analysis of zooplankton communities in over 1,100 water bodies spanning the Western Hemisphere (7... more Analysis of zooplankton communities in over 1,100 water bodies spanning the Western Hemisphere (778S, 818N latitude) revealed latitudinal patterns in cladoceran body size and Daphnia seasonal dynamics. The mean body length of cladoceran species occurring at different latitudinal intervals was greatest in north temperate regions, declining in size toward the poles and equator. Thus, mean cladoceran size was greatest in
... JF Gillooly and SI Dodson Department of Zoology, 430 Lincoln Drive, University of Wisconsin, ... more ... JF Gillooly and SI Dodson Department of Zoology, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA (Accepted 18 August 1999) ... We also thank Matthew Brewer, Bill Karasov, and Chris Tracy for critically reading the manuscript. ...
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Papers by James Gillooly