Metabolic scaling has diversified among species, despite an evolutionary constraint within species
Preprint posted on 29 May 2020 https://www.biorxiv.org/content/10.1101/2020.05.26.117846v1
Ontogenetic metabolic scaling slopes exhibit considerable phenotypic variability, but phylogenetic analysis reveals evolutionary constraints prevail
Selected by Charlotte Nelson
Categories: developmental biology, ecology, evolutionary biology, genetics, physiology, zoology
Background
Since the pioneering work of Kleiber (and others) in the early 1900’s we have known that metabolic rate appears to scale allometrically with body size; larger animals have a lower metabolic rate per unit body mass. Yet despite almost a century of work, the underlying mechanisms and their importance for the fixed physical constraints on metabolic scaling remain up for debate. In theory, macroevolutionary patterns arise as a result of microevolutionary processes (drift, mutation, recombination, selection), however empirical data which would enable the assessment of how these processes contribute to variation in metabolic scaling is still lacking. In addition, much of the previous literature has focussed on investigating these factors in adult animals due to the additional complications of estimating standard metabolic rate in the developing animal.
There have been several recent studies estimating the additive genetic variance for metabolic rate and mass as separate traits. This is somewhat surprising considering that these traits usually exhibit strong, positive genetic correlation. Such persistent association between these traits suggests that they may share loci, or that the loci underlying them exhibit linkage disequilibrium. We know that genetically correlated traits do not evolve independently, thereby affecting short term evolutionary responses to phenotypic selection. However, on the extended timescales over which speciation occurs, the genetic relationships between traits may be altered by directional and stabilising selection. By investigating the patterns of genetic variation in the relationship between mass and metabolic rate Beaman and co-authors aimed to identify the evolutionary constraints on metabolic scaling through development, and also attempt to understand how the microevolutionary processes involved contribute to the basis and maintenance of metabolic allometry.
Metabolic scaling through development
Evolutionary responses to selection obviously necessitate a heritable genetic basis to the variation observed in the trait. Until now, no studies have been able to rigorously assess how much of the variation observed in ontogenetic metabolic scaling slopes is due to heritable genetic effects while at the same time accounting for other known sources of variation which may confound heritability estimates. In this preprint, Beaman et al, used a large scale quantitative genetic study to investigate the evolutionary constraints on ontogenetic metabolic scaling in speckled cockroaches (N. cinera). Phenotypic traits (resting metabolic rate, mass) were measured repeatedly in more than 1200 individuals of known parentage throughout their development. This study shows that metabolic scaling slope and intercept are not static quantities but display phenotypic variation which arises from maternal affects (and other unaccounted for sources of variation), however are not impacted by additive genetic variance. This is a novel result as no previous studies have attempted to estimate the heritability of metabolic scaling relationships. Consequently, it appears that ontogenetic metabolic scaling is not phenotypically fixed, however does seem to be evolutionarily constrained within species.
Figure 1: Metabolic rate and mass measurements repeated across ontogeny in speckled cockroaches. Points show individual paired measurements, black lines show maternal effect variance in the ontogenetic metabolic scaling relationship. Preprint figure 3.
Phylogenetic analysis of scaling
Additionally, they used phylogenetic analysis of an existing data set (Glazier, 2005) to investigate differences in ontogenetic metabolic scaling between species and tested whether grouping by; endothermic vs ectothermic, vertebrate vs invertebrate, aquatic vs amphibian vs terrestrial, explained variance in scaling slopes independent of phylogenetic location.
Analysis of the ontogenetic metabolic scaling data presented by Glazier et al (2005) showed that there is considerable variability in scaling slope among species, ranging from around 0.4 to 1.0. Despite such variation, Beaman et alsuggest that the ontogenetic scaling slopes are more similar between closely relative species; a finding that is consistent with the existence of a heritable basis to metabolic allometry. However, it is important to consider that more closely related species may be more likely to share similar environmental conditions (e.g. habitat type, nutrition, temperature) which could potentially manufacture a link between metabolic scaling slope and relatedness. In order to test this, Beaman et al, then grouped species by various aspects of physiology and ecology (endotherms vs ectotherms, vertebrates vs invertebrates, aquatic vs amphibious vs terrestrial) and found no consistent differences in scaling slope between any groupings. Consequently, it is still unclear which factors drive between species variation in ontogenetic metabolic scaling slopes, but the authors speculate that variation in energy demanding processes e.g. activity and development, or abiotic factors e.g. temperature, may be of importance. It is therefore concluded that the constraints acting upon metabolic scaling are likely subject to change during lineage diversification.
What’s next?
The authors conclude that there appears to be strong stabilising selection acting on the combination of mass and metabolic rate within species. While it would be fascinating to link individual variation in the underlying functional mechanisms to variations in fitness to determine how these mechanisms are exposed to selection at the whole organism level, it would require a prohibitively large phenotyping effort. Currently it is more practical to study how the covariation in mass and metabolic rate at the whole organism level is associated with variations in fitness using high throughput metabolic rate phenotyping. Beaman et al,hypothesize that there is strong stabilising selection on the combination of mass and metabolic rate within populations which favours a positive correlation between these traits with an allometric slope of less than one.
Overall, I really enjoyed the approach and ideas behind the questions tackled in this preprint. While the literature on metabolic scaling is vast, that focussed on metabolic scaling during development lags behind and it’s refreshing to see these gaps start to be filled. The scale of metabolic trait measurement in this work is also commendable; with over 1500 individual metabolic rate measurements conducted this work represents one of the largest sampling efforts ever conducted for this type of physiological trait.
Open questions
1) Often the ontogenetic scaling factor is closer to 1 due to growth, why do you think you calculated a much lower value here?
2) To what extent could epigenetic factors be playing a role in the constraint/modulation of metabolic scaling factors?
3) There appears to be a slight pinch point in variation in mass specific metabolic rate in the cockroaches at around 150 mg – do you have any ideas about what may be causing this?
Additional references
Glazier, D. S. (2005). Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biological reviews, 80, 611-662.
Kleiber, M. (1932). Body size and metabolism. Hilgardia 6 (11), 315-353.
Posted on: 30 June 2020
doi: https://doi.org/10.1242/prelights.22419
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