Universal rules of life: metabolic rates, biological times and the equal fitness paradigm

Burger, Joseph R.; Hou, Chen; Hall, Charles A. S.; Brown, James H.

doi:10.1111/ele.13715

Cited by 51 publications

(43 citation statements)

References 171 publications

(292 reference statements)

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“…Such long-term experiments would need to quantify the cascading effects of varying the strength of resource competition on sex-specific life histories, metabolic phenotypes, the economics of mating, and mating system parameters. Further, in systems where this is possible, quantitative analyses explicitly based on mass–energy balance considerations and the bio-physical constraints that dictate resource acquisition and allocation ( 119 – 121 ) could provide further insights.…”

Section: Discussionmentioning

confidence: 99%

Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles

Arnqvist

Rönn

Watson

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Male–female coevolution has taken different paths among closely related species, but our understanding of the factors that govern its direction is limited. While it is clear that ecological factors, life history, and the economics of reproduction are connected, the divergent links are often obscure. We propose that a complete understanding requires the conceptual integration of metabolic phenotypes. Metabolic rate, a nexus of life history evolution, is constrained by ecological factors and may exert important direct and indirect effects on the evolution of sexual dimorphism. We performed standardized experiments in 12 seed beetle species to gain a rich set of sex-specific measures of metabolic phenotypes, life history traits, and the economics of mating and analyzed our multivariate data using phylogenetic comparative methods. Resting metabolic rate (RMR) showed extensive evolution and evolved more rapidly in males than in females. The evolution of RMR was tightly coupled with a suite of life history traits, describing a pace-of-life syndrome (POLS), with indirect effects on the economics of mating. As predicted, high resource competition was associated with a low RMR and a slow POLS. The cost of mating showed sexually antagonistic coevolution, a hallmark of sexual conflict. The sex-specific costs and benefits of mating were predictably related to ecology, primarily through the evolution of male ejaculate size. Overall, our results support the tenet that resource competition affects metabolic processes that, in turn, have predictable effects on both life history evolution and reproduction, such that ecology shows both direct and indirect effects on male–female coevolution.

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Section: Discussionmentioning

confidence: 99%

Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles

Arnqvist

Rönn

Watson

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Evolution promotes a duality of uniqueness and universality ( 55 ). While organismal diversity is a primary outcome of natural selection within distinct environments, there is a paradoxical preservation of shared, fundamental functions across species.…”

Section: Discussionmentioning

confidence: 99%

CD36 homologs determine microbial resistance to the Lyme disease spirochete

O’Neal

Singh

Forrest

et al. 2022

Preprint

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Pattern recognition receptors sense pathogens in arthropods and mammals through distinct immune processes. Whether these molecules share a similar function and recognize the same microbe in evolutionarily distant species remain ill-defined. Here, we establish that the CD36 superfamily is required for Borrelia burgdorferi resistance in both the arthropod vector and humans. Using the blacklegged tick Ixodes scapularis and an electronic health record-linked biobank, we demonstrate that CD36 members elicit immunity to the Lyme disease spirochete. In ticks, the CD36-like protein Croquemort recognizes lipids and initiates the immune deficiency and jun N-terminal kinase pathways against B. burgdorferi. In humans, exome sequencing and clinical information reveal that individuals with CD36 loss-of-function variants have increased prevalence of Lyme disease. Altogether, we discovered a conserved mechanism of anti-bacterial immunity.

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“…The equal fitness paradigm (EFP: Brown et al 2018 ; updated and extended: Burger et al 2019 , 2021 ; Brown et al 2022 ) provides a biophysical foundation for the central importance of energy in life history, ecology, and evolution. With stable populations and biodiversity, all species regardless of size are equally fit, because parents transfer equal quantities of energy and biomass to surviving offspring in the next generation.…”

Section: The Need For Better Field Data On Life-history Variables Rel...mentioning

confidence: 99%

“…Most studies of metabolic scaling have used laboratory data, but Equation 1 and all biotic interaction hypotheses focus on interactions in the field. Therefore, priorities for empirical research should include more and better data on P coh , G , and F in the field ( Burger et al 2021 ). Comparisons of wild, managed, and domesticated animal populations, and artificial systems in which species can evolve in competition with each other will be useful for evaluating biotic interaction hypotheses and the EFP.…”

Section: The Need For Better Field Data On Life-history Variables Rel...mentioning

confidence: 99%

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals

Harrison

Biewener

Bernhardt

et al. 2022

Integrative and Comparative Biology

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Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

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Universal rules of life: metabolic rates, biological times and the equal fitness paradigm

Cited by 51 publications

References 171 publications

Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles

Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles

CD36 homologs determine microbial resistance to the Lyme disease spirochete

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals

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