Metabolic scaling of individuals vs. populations: Evidence for variation in scaling exponents at different hierarchical levels

Biological allometries, such as the scaling of metabolism to mass, are hypothesized to result from natural selection to maximize how vascular networks fill space yet minimize internal transport distances and resistance to blood flow. Metabolic scaling theory argues two guiding principles—conservation of fluid flow and space-filling fractal distributions—describe a diversity of biological networks and predict how the geometry of these networks influences organismal metabolism. Yet, mostly absent from past efforts are studies that directly, and independently, measure metabolic rate from respiration and vascular architecture for the same organ, organism, or tissue. Lack of these measures may lead to inconsistent results and conclusions about metabolism, growth, and allometric scaling. We present simultaneous and consistent measurements of metabolic scaling exponents from clinical images of lung cancer, serving as a first-of-its-kind test of metabolic scaling theory, and identifying potential quantitative imaging biomarkers indicative of tumor growth. We analyze data for 535 clinical PET-CT scans of patients with non-small cell lung carcinoma to establish the presence of metabolic scaling between tumor metabolism and tumor volume. Furthermore, we use computer vision and mathematical modeling to examine predictions of metabolic scaling based on the branching geometry of the tumor-supplying blood vessel networks in a subset of 56 patients diagnosed with stage II-IV lung cancer. Examination of the scaling of maximum standard uptake value with metabolic tumor volume, and metabolic tumor volume with gross tumor volume, yield metabolic scaling exponents of 0.64 (0.20) and 0.70 (0.17), respectively. We compare these to the value of 0.85 (0.06) derived from the geometric scaling of the tumor-supplying vasculature. These results: (1) inform energetic models of growth and development for tumor forecasting; (2) identify imaging biomarkers in vascular geometry related to blood volume and flow; and (3) highlight unique opportunities to develop and test the metabolic scaling theory of ecology in tumors transitioning from avascular to vascular geometries.

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Testing allometric scaling relationships in plant roots

Forest Ecosystems ◽

10.1186/s40663-020-00269-6 ◽

2020 ◽

Vol 7 (1) ◽

Author(s):

Qiang Deng ◽

Zhiyou Yuan ◽

Xinrong Shi ◽

T. Ryan Lock ◽

Robert L. Kallenbach

Keyword(s):

Plant Root ◽

Woody Species ◽

Plant Roots ◽

Scaling Exponent ◽

Terrestrial Plants ◽

Natural Habitats ◽

Scaling Exponents ◽

Coarse Roots ◽

Metabolic Scaling ◽

Metabolic Scaling Theory

Abstract Background Metabolic scaling theory predicts that plant productivity and biomass are both size-dependent. However, this theory has not yet been tested in plant roots. Methods In this study, we tested how metabolic scaling occurs in plants using a comprehensive plant root dataset made up of 1016 observations from natural habitats. We generated metabolic scaling exponents by log-transformation of root productivity versus biomass. Results Results showed that the metabolic scaling exponents of fine root (< 2 mm in diameter) productivity versus biomass were close to 1.0 for all ecosystem types and functional groups. Scaling exponents decreased in coarse roots (> 2 mm in diameter). Conclusions We found isometric metabolic scaling in fine roots, a metabolically active organ similar to seedlings or saplings. Our findings also indicate a shift in metabolic scaling during plant development. Overall, our study supports the absence of any unified single constant scaling exponent for metabolism-biomass relationships in terrestrial plants, especially for forests with woody species.

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Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2006.3741 ◽

2006 ◽

Vol 274 (1608) ◽

pp. 431-438 ◽

Cited By ~ 144

Author(s):

Shaun S Killen ◽

Isabel Costa ◽

Joseph A Brown ◽

A. Kurt Gamperl

Keyword(s):

Fish Species ◽

Fish Larvae ◽

Developmental Trajectory ◽

Early Life Stages ◽

Aerobic Scope ◽

Scaling Exponents ◽

Metabolic Scaling ◽

Aerobic Activity ◽

The Relationship ◽

Limited Scope

Fish larvae are the world's smallest vertebrates, and their high rates of mortality may be partially owing to a very limited aerobic scope. Unfortunately, however, no complete empirical dataset exists on the relationship between minimal and maximal metabolism (and thus aerobic scope) for any fish species throughout ontogeny, and thus such an association is hard to delineate. We measured standard and maximal metabolism in three marine fish species over their entire life history, and show that while aerobic scope depends greatly on body size and developmental trajectory, it is extremely small during the early life stages (factorial aerobic scope≤1.5). Our findings strongly suggest that limited scope for aerobic activity early in life is likely to constrain physiological function and ultimately impact behaviour and possibly survival. Furthermore, our results have important implications for ecological models that incorporate metabolic scaling, and provide additional evidence against the existence of ‘universal’ scaling exponents.

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Estimating architecture-based metabolic scaling exponents of tropical trees using terrestrial LiDAR and 3D modelling

Forest Ecology and Management ◽

10.1016/j.foreco.2019.02.019 ◽

2019 ◽

Vol 439 ◽

pp. 132-145 ◽

Cited By ~ 8

Author(s):

Alvaro Lau ◽

Christopher Martius ◽

Harm Bartholomeus ◽

Alexander Shenkin ◽

Tobias Jackson ◽

...

Keyword(s):

Tropical Trees ◽

3D Modelling ◽

Scaling Exponents ◽

Terrestrial Lidar ◽

Metabolic Scaling

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Adaptive diversification of growth allometry in the plant Arabidopsis thaliana

10.1101/269498 ◽

2018 ◽

Cited By ~ 2

Author(s):

François Vasseur ◽

Moises Exposito-Alonso ◽

Oscar Ayala-Garay ◽

George Wang ◽

Brian J. Enquist ◽

...

Keyword(s):

Growth Rate ◽

Arabidopsis Thaliana ◽

Abiotic Stress ◽

Seed Production ◽

Allometric Scaling ◽

Abiotic Stress Response ◽

Scaling Exponents ◽

Metabolic Scaling ◽

Metabolic Scaling Theory ◽

Growth Scaling

AbstractSeed plants vary tremendously in size and morphology. However, variation and covariation between plant traits may at least in part be governed by universal biophysical laws and biological constants. Metabolic Scaling Theory (MST) posits that whole-organismal metabolism and growth rate are under stabilizing selection that minimizes the scaling of hydrodynamic resistance and maximizes the scaling of resource uptake. This constrains variation in physiological traits and in the rate of biomass accumulation, so that they can be expressed as mathematical functions of plant size with near constant allometric scaling exponents across species. However, observed variation in scaling exponents questions the evolutionary drivers and the universality of allometric equations. We have measured growth scaling and fitness traits of 451 Arabidopsis thaliana accessions with sequenced genomes. Variation among accessions around the scaling exponent predicted by MST correlated with relative growth rate, seed production and stress resistance. Genomic analyses indicate that growth allometry is affected by many genes associated with local climate and abiotic stress response. The gene with the strongest effect, PUB4, has molecular signatures of balancing selection, suggesting that intraspecific variation in growth scaling is maintained by opposing selection on the trade-off between seed production and abiotic stress resistance. Our findings support a core MST prediction and suggest that variation in allometry contributes to local adaptation to contrasting environments. Our results help reconcile past debates on the origin of allometric scaling in biology, and begin to link adaptive variation in allometric scaling to specific genes.Significance statementAre there biological constants unifying phenotypic diversity across scales? Metabolic Scaling Theory (MST) predicts mathematical regularity and constancy in the allometric scaling of growth rate with body size across species. Here, we show that adaptation to climate in Arabidopsis thaliana is associated with local strains that substantially deviate from the values predicted by MST. This deviation can be linked to increased stress tolerance at the expense of seed production, and it occurs through selection on genes that are involved in abiotic stress response and that are geographically correlated with climatic conditions. This highlights the evolutionary role of allometric diversification and helps establish the physiological bases of plant adaptation to contrasting environments.

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Major evolutionary transitions of life, metabolic scaling and the number and size of mitochondria and chloroplasts

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0611 ◽

2016 ◽

Vol 283 (1831) ◽

pp. 20160611 ◽

Cited By ~ 12

Author(s):

Jordan G. Okie ◽

Val H. Smith ◽

Mercedes Martin-Cereceda

Keyword(s):

Cell Volume ◽

Cell Size ◽

Cellular Metabolism ◽

Eukaryotic Cells ◽

Free Living ◽

Scaling Exponents ◽

Evolutionary Transitions ◽

Metabolic Scaling ◽

Discernible Effect ◽

Evolutionary Transitions In Individuality

We investigate the effects of trophic lifestyle and two types of major evolutionary transitions in individuality—the endosymbiotic acquisition of organelles and development of multicellularity—on organellar and cellular metabolism and allometry. We develop a quantitative framework linking the size and metabolic scaling of eukaryotic cells to the abundance, size and metabolic scaling of mitochondria and chloroplasts and analyse a newly compiled, unprecedented database representing unicellular and multicellular cells covering diverse phyla and tissues. Irrespective of cellularity, numbers and total volumes of mitochondria scale linearly with cell volume, whereas chloroplasts scale sublinearly and sizes of both organelles remain largely invariant with cell size. Our framework allows us to estimate the metabolic scaling exponents of organelles and cells. Photoautotrophic cells and organelles exhibit photosynthetic scaling exponents always less than one, whereas chemoheterotrophic cells and organelles have steeper respiratory scaling exponents close to one. Multicellularity has no discernible effect on the metabolic scaling of organelles and cells. In contrast, trophic lifestyle has a profound and uniform effect, and our results suggest that endosymbiosis fundamentally altered the metabolic scaling of free-living bacterial ancestors of mitochondria and chloroplasts, from steep ancestral scaling to a shallower scaling in their endosymbiotic descendants.

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