Understanding variation in metabolic rate

Authors: Amanda K Pettersen, Dustin J Marshall, and Craig R White

Published in: The Journal of Experimental Biology

Abstract

Metabolic rate reflects an organism’s capacity for growth, maintenance and reproduction, and is likely to be a target of selection. Physiologists have long sought to understand the causes and consequences of within-individual to among-species variation in metabolic rates – how metabolic rates relate to performance and how they should evolve.

Traditionally, this has been viewed from a mechanistic perspective, relying primarily on hypothesis-driven approaches. A more agnostic, but ultimately more powerful tool for understanding the dynamics of phenotypic variation is through use of the breeder’s equation, because variation in metabolic rate is likely to be a consequence of underlying microevolutionary processes.

Here we show that metabolic rates are often significantly heritable, and are therefore free to evolve under selection. We note, however, that ‘metabolic rate’ is not a single trait: in addition to the obvious differences between metabolic levels (e.g. basal, resting, free-living, maximal), metabolic rate changes through ontogeny and in response to a range of extrinsic factors, and is therefore subject to multivariate constraint and selection.

We emphasize three key advantages of studying metabolic rate within a quantitative genetics framework: its formalism, and its predictive and comparative power.

We make several recommendations when applying a quantitative genetics framework: (i) measuring selection based on actual fitness, rather than proxies for fitness; (ii) considering the genetic covariances between metabolic rates throughout ontogeny; and (iii) estimating genetic covariances between metabolic rates and other traits.

A quantitative genetics framework provides the means for quantifying the evolutionary potential of metabolic rate and why variance in metabolic rates within populations might be maintained.

Pettersen AK, Marshall DJ, White CR (2018) Understanding variation in metabolic rate, The Journal of Experimental Biology, PDF DOI

Eco-energetic consequences of evolutionary shifts in body size

Authors: Martino E Malerba, Craig R White, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Size imposes physiological and ecological constraints upon all organisms. Theory abounds on how energy flux covaries with body size, yet causal links are often elusive.

As a more direct way to assess the role of size, we used artificial selection to evolve the phytoplankton species Dunaliella tertiolecta towards smaller and larger body sizes.

Within 100 generations (c. 1 year), we generated a fourfold difference in cell volume among selected lineages. Large-selected populations produced four times the energy than small-selected populations of equivalent total biovolume, but at the cost of much higher volume-specific respiration. These differences in energy utilisation between large (more productive) and small (more energy-efficient) individuals were used to successfully predict ecological performance (r and K) across novel resource regimes.

We show that body size determines the performance of a species by mediating its net energy flux, with worrying implications for current trends in size reduction and for global carbon cycles.

Malerba ME, White CR, Marshall DJ (2017) Eco-energetic consequences of evolutionary shifts in body size, Ecology Letters, PDF DOI 

Does the cost of development scale allometrically with offspring size?

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson-Richardson, and Dustin J Marshall

Published in: Functional Ecology

Summary

Within many species, larger offspring have higher fitness. While the presence of an offspring size-fitness relationship is canonical in life-history theory, the mechanisms that determine why this relationship exists are unclear.

Linking metabolic theory to life-history theory could provide a general explanation for why larger offspring often perform better than smaller offspring. In many species, energy reserves at the completion of development drive differences in offspring fitness. Development is costly so any factor that decreases energy expenditure during development should result in higher energy reserves and thus subsequently offspring fitness.

Metabolic theory predicts that larger offspring should have relatively lower metabolic rates and thus emerge with a higher level of energy reserves (assuming developmental times are constant). The increased efficiency of development in larger offspring may therefore be an underlying driver of the relationship between offspring size and offspring fitness, but this has not been tested within species.

To determine how the costs of development scale with offspring size, we measured energy expenditure throughout development in the model organism Danio rerio across a range of natural offspring sizes. We also measured how offspring size affects the length of the developmental period. We then examined how hatchling size and condition scale with offspring size.

We find that larger offspring have lower mass-specific metabolic rates during development, but develop at the same rate as smaller offspring. Larger offspring also hatch relatively heavier and in better condition than smaller offspring. That the relative costs of development decrease with offspring size may provide a widely applicable explanation for why larger offspring often perform better than smaller offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2017) Does the cost of development scale allometrically with offspring size?, Functional Ecology, PDF DOI 

Does energy flux predict density-dependence? An empirical field test

Authors: Giulia Ghedini, Craig R White, and Dustin J Marshall

Published in: Ecology

Abstract

Changes in population density alter the availability, acquisition and expenditure of resources by individuals, and consequently their contribution to the flux of energy in a system.

Whilst both negative and positive density-dependence have been well studied in natural populations, we are yet to estimate the underlying energy flows that generate these patterns and the ambivalent effects of density make prediction difficult.

Ultimately, density-dependence should emerge from the effects of conspecifics on rates of energy intake (feeding) and expenditure (metabolism) at the organismal level, thus determining the discretionary energy available for growth.

Using a model system of colonial marine invertebrates, we measured feeding and metabolic rates across a range of population densities to calculate how discretionary energy per colony changes with density and test whether this energy predicts observed patterns in organismal size across densities.

We found that both feeding and metabolic rates decline with density but that feeding declines faster, and that this discrepancy is the source of density-dependent reductions in individual growth. Importantly, we could predict the size of our focal organisms after 8 weeks in the field based on our estimates of energy intake and expenditure.

The effects of density on both energy intake and expenditure overwhelmed the effects of body size; even though higher density populations had smaller colonies (with higher mass-specific biological rates), density effects meant that these smaller colonies had lower mass-specific rates overall.

Thus, to predict the contribution of organisms to the flux of energy in populations it seems necessary not only to quantify how rates of energy intake and expenditure scale with body size, but also how they scale with density given that this ecological constraint can be a stronger driver of energy use than the physiological constraint of body size.

Ghedini G, White CR, Marshall DJ (2017) Does energy flux predict density-dependence? An empirical field test. Ecology, PDF DOI

Phytoplankton size-scaling of net-energy flux across light and biomass gradients

Authors: Martino E Malerba, Craig R White, and Dustin J Marshall

Published in: Ecology

Abstract

Changes in population density alter the availability, acquisition and expenditure of resources by individuals, and consequently their contribution to the flux of energy in a system.

Whilst both negative and positive density-dependence have been well studied in natural populations, we are yet to estimate the underlying energy flows that generate these patterns and the ambivalent effects of density make prediction difficult. Ultimately, density-dependence should emerge from the effects of conspecifics on rates of energy intake (feeding) and expenditure (metabolism) at the organismal level, thus determining the discretionary energy available for growth.

Using a model system of colonial marine invertebrates, we measured feeding and metabolic rates across a range of population densities to calculate how discretionary energy per colony changes with density and test whether this energy predicts observed patterns in organismal size across densities.

We found that both feeding and metabolic rates decline with density but that feeding declines faster, and that this discrepancy is the source of density-dependent reductions in individual growth. Importantly, we could predict the size of our focal organisms after 8 weeks in the field based on our estimates of energy intake and expenditure. The effects of density on both energy intake and expenditure overwhelmed the effects of body size; even though higher density populations had smaller colonies (with higher mass-specific biological rates), density effects meant that these smaller colonies had lower mass-specific rates overall.

Thus, to predict the contribution of organisms to the flux of energy in populations it seems necessary not only to quantify how rates of energy intake and expenditure scale with body size, but also how they scale with density given that this ecological constraint can be a stronger driver of energy use than the physiological constraint of body size.

Malerba ME, White C, Marshall DJ (2017) Phytoplankton size-scaling of net-energy flux across light and biomass gradients. Ecology PDF DOI

Low-carbohydrate diet induces metabolic depression: a possible mechanism to conserve glycogen

Authors: Hugh S Winwood-Smith, Craig E Franklin, and Craig R White

Published in: American Journal of Physiology – Regulatory, Integrative and Comparative Physiology, volume 313, number 4

Abstract

Long-term studies have found that low-carbohydrate diets are more effective for weight loss than calorie-restricted diets in the short term but equally or only marginally more effective in the long term. Low-carbohydrate diets have been linked to reduced glycogen stores and increased feeling of fatigue.

We propose that reduced physical activity in response to lowered glycogen explains the diminishing weight loss advantage of low-carbohydrate compared with low-calorie diets over longer time periods.

We explored this possibility by feeding adult Drosophila melanogaster a standard or a low-carbohydrate diet for 9 days and measured changes in metabolic rate, glycogen stores, activity, and body mass.

We hypothesized that a low-carbohydrate diet would cause a reduction in glycogen stores, which recover over time, a reduction in physical activity, and an increase in resting metabolic rate.

The low-carbohydrate diet reduced glycogen stores, which recovered over time. Activity was unaffected by diet, but metabolic rate was reduced, in the low-carbohydrate group.

We conclude that metabolic depression could explain the decreased effectiveness of low-carbohydrate diets over time and recommend further investigation of long-term metabolic effects of dietary interventions and a greater focus on physiological plasticity within the study of human nutrition.

Winwood-Smith HS, Franklin CE, White CR (2017) Low-carbohydrate diet induces metabolic depression: a possible mechanism to conserve glycogen, American Journal of Physiology – Regulatory, Integrative and Comparative PhysiologyPDF DOI 

Research fellow position: Adaptive Dynamics Modeller

  • Level A, research-only academic
  • $64,450 to $87,471 pa + 9.5% superannuation
  • Full-time, starting late 2017
  • Two-year, fixed-term
  • Monash University Clayton campus

The Centre for Geometric Biology is currently seeking to recruit an experienced theoretical biologist experienced in adaptive dynamics modelling.

As the postdoctoral researcher, you will use adaptive dynamics modelling approaches to explore the drivers and consequences of body size evolution. Working with other researchers in the Centre for Geometric Biology, you will parameterise models based on empirical findings and provide advice of key tests of model predictions.

You will further be expected to maintain consistently high research output in the form of quality publications, supervision of students, development and submission of grant proposals to external funding agencies, contribute more generally to communicating the research activities of the group, and participation in appropriate career development activities.

Key selection criteria

  1. A degree in a relevant area, utilising adaptive dynamics approaches, from a recognised university with subsequent relevant work experience, or an equivalent combination of experience and training.
  2. Demonstrated experience in developing theoretical models in fundamental ecology or empirical research using cutting-edge quantitative approaches.
  3. Demonstrated ability to undertake outstanding research; with a high quality research publication record in recognised journals.
  4. Ability to solve problems by using discretion, innovation and the exercise of high level diagnostic skills within areas of functional responsibility or professional expertise.
  5. Excellent written communication and verbal communication skills with proven ability to effectively analyse information and produce clear, succinct reports and documents which requires interaction with others.
  6. Demonstrated planning and organisational skills, with the ability to prioritise multiple tasks and set and meet deadlines.
  7. Demonstrated awareness of the principles of confidentiality, privacy and information handling.
  8. Demonstrated ability to effectively work independently and in a multidisciplinary team to make a contribution to research and scholarship.
  9. Experience of, or willingness to work on, marine systems.
  10. A demonstrated understanding of questions in fundamental ecology and/or evolution.

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

For more information, or to apply, refer to the Monash University website