Metabolic scaling is the product of life-history optimization

White, Craig R.; Alton, Lesley A.; Bywater, Candice L.; Lombardi, Emily J; Marshall, Dustin J.

doi:10.1126/science.abm7649

Cited by 119 publications

(120 citation statements)

References 65 publications

(91 reference statements)

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“…In a scenario like the K-Pg extinction, during which networks of ecological competition were reset [53], the survivorship of clades with smaller body sizes-and therefore weaker associations between metabolic rate and body massmay have facilitated the rapid evolution of a range of physiological strategies in the early Cenozoic (e.g., [54][55][56]). This result is consistent with theoretical advances predicting that transitions toward harsher environments with increased extrinsic mortality will result in the evolution of lower metabolic scaling exponents because of selection to maximize lifetime reproduction [57]. In turn, this phenomenon leads to earlier maturation and more rapid growth [57], consistent with our inference of shifts toward altriciality associated with the K-Pg extinction (e.g., [47,58,59]).…”

Section: Discussionsupporting

confidence: 91%

“…This result is consistent with theoretical advances predicting that transitions toward harsher environments with increased extrinsic mortality will result in the evolution of lower metabolic scaling exponents because of selection to maximize lifetime reproduction [57]. In turn, this phenomenon leads to earlier maturation and more rapid growth [57], consistent with our inference of shifts toward altriciality associated with the K-Pg extinction (e.g., [47,58,59]).…”

Section: Discussionsupporting

confidence: 91%

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Molecular early burst associated with the diversification of birds at the K–Pg boundary

Berv

Singhal

Field

et al. 2022

Preprint

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Complex patterns of genome and life-history evolution associated with the end-Cretaceous (K– Pg) mass extinction event limit our understanding of the early evolutionary history of crown group birds. Here, we assess molecular heterogeneity across living birds using a technique enabling inferred sequence substitution models to transition across the history of a clade. Our approach identifies contrasting patterns among exons, introns, untranslated regions, and mitochondrial genomes that reflect distinct regimes of molecular evolution. Up to fifteen shifts in the mode of avian molecular evolution map to rapidly diversifying clades near the Cretaceous-Palaeogene boundary, demonstrating a burst of genomic disparity early in the evolutionary history of crown birds. Using simulation and machine learning techniques, we show that shifts in developmental mode or adult body mass best explain transitions in the mode of nucleotide substitution. These patterns are related, in turn, to macroevolutionary shifts in the allometric scaling relationship between basal metabolic rate and body mass. In agreement with theoretical predictions, we show that this scaling relationship became weaker across the end-Cretaceous transition. Ultimately, our study provides evidence that the Chicxulub bolide impact triggered integrated patterns of evolution across avian genomes, physiology, and life history that structured the evolutionary potential of modern birds.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 91%

Molecular early burst associated with the diversification of birds at the K–Pg boundary

Berv

Singhal

Field

et al. 2022

Preprint

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“…The copyright holder for this this version posted October 21, 2022. ; https://doi.org/10.1101/2022.10.19.512836 doi: bioRxiv preprint 12 history optimization influences the coexistence of coadapted species through changes in their metabolic scaling. Understanding how metabolism, size, and demography covary between competing species is essential to explain patterns of biological production and extrapolate the effect of biodiversity over time (1,22).…”

Section: Discussionmentioning

confidence: 99%

Metabolic evolution in response to interspecific competition in a eukaryote

Ghedini

Marshall

2022

Preprint

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SummarySpecies traits can evolve rapidly in response to competition, influencing the diversity and productivity of communities. Metabolic and life history theories both predict how competition should affect metabolism, size, and demography. However, these predictions are based on indirect evidence from macroevolutionary patterns or among-species comparisons. Direct experimental tests are rare and mostly focused on single or pairs of species, so how species evolve in communities is unclear, particularly in eukaryotes. We use experimental evolution of eukaryotic marine phytoplankton to examine how metabolism, size, and demography coevolve under competition. Specifically, we compare the traits of a focal species that evolved either alone, with intraspecific competitors or with a community at two points in time. We find that the focal species evolved both size and metabolism under competition, which led to an increase in carrying capacity as in max. population density. These demographic changes were predicted by classic metabolic theory based on the species-specific scaling of metabolism with size. However, we also find important departures from theory. Evolution led to Pareto improvements in both population growth rate and carrying capacity, so the existence of classic r-K trade-offs seems less inevitable than what suggested by among-species comparisons. The finding that both intra- and inter-specific competition maximize carrying capacity through changes in size and metabolism could have important consequences for our ability to predict evolution in communities.

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“…Importantly, these observations highlight the deep connections between multiple phenotypic layers of multicellular systems and argue for a broader ‘phenomics’ perspective (Gandara et al, 2022), instead of a strictly gene-centric view. In the future, exploring the interplay of metabolic and developmental networks could transform our understanding of evolution and development across variable ecologies (Miyazawa and Aulehla, 2018; Perkins et al, 2022), as such processes are fundamentally linked (White et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

Rapid response of fly populations to gene dosage across development and generations

Li¹,

Gándara²,

Ekelof³

et al. 2022

Preprint

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It remains unknown how developmental systems evolve in response to variable genetic and environmental conditions. Here, we have examined the evolvability of the classic bicoid network in Drosophila, which is essential for anterior-posterior patterning in the early embryo. This network can be synthetically perturbed by increasing the dosage of bicoid, which causes a posterior shift of the network's regulatory outputs and a decrease in fitness. To directly monitor network evolution across populations with extra copies of bicoid, we performed genome-wide EMS mutagenesis, followed by experimental evolution. After only 8-15 generations, evolved populations have normalized patterns of gene expression and increased survival. Using a phenomics approach, we find that populations normalized through rapid increases in embryo size driven by maternal changes in metabolism and ovariole development. We extend our results to wild populations of flies, demonstrating strong predictability. Together, our results necessitate a broader view of regulatory network evolution at the systems level. This study highlights the power of synthetic evolution using animal systems, a generalizable platform for the dissection of gene regulation and complex genomes.

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Metabolic scaling is the product of life-history optimization

Cited by 119 publications

References 65 publications

Molecular early burst associated with the diversification of birds at the K–Pg boundary

Molecular early burst associated with the diversification of birds at the K–Pg boundary

Metabolic evolution in response to interspecific competition in a eukaryote

Rapid response of fly populations to gene dosage across development and generations

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