Beneficial mutations from evolution experiments increase rates of growth and fermentation

Authors: Aysha L Sezmis, Martino E Malerba, Dustin J Marshall and Michael J McDonald

Published in: Journal of Molecular Evolution, volume 86, issue 2 (February 2018)

A major goal of evolutionary biology is to understand how beneficial mutations translate into increased fitness.

Here, we study beneficial mutations that arise in experimental populations of yeast evolved in glucose-rich media. We find that fitness increases are caused by enhanced maximum growth rate (R) that come at the cost of reduced yield (K).

We show that for some of these mutants, high R coincides with higher rates of ethanol secretion, suggesting that higher growth rates are due to an increased preference to utilize glucose through the fermentation pathway, instead of respiration. We examine the performance of mutants across gradients of glucose and nitrogen concentrations and show that the preference for fermentation over respiration is influenced by the availability of glucose and nitrogen.

Overall, our data show that selection for high growth rates can lead to an enhanced Crabtree phenotype by the way of beneficial mutations that permit aerobic fermentation at a greater range of glucose concentrations.

Citation

Sezmis AL, Malerba ME, Marshall DJ, McDonald MJ (2018) Beneficial mutations from evolution experiments increase rates of growth and fermentation, Journal of Molecular Evolution, PDF 964 KB doi:10.1007/s00239-018-9829-9

Understanding variation in metabolic rate

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

Published in: The Journal of Experimental Biology, volume 221, number 1 (January 2018)

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.

Citation

Pettersen AK, Marshall DJ, White CR (2018) Understanding variation in metabolic rate., The Journal of Experimental Biology, PDF 596 KB doi:10.1242/jeb.166876

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.

Citation

Malerba ME, White CR, Marshall DJ (2017) Eco-energetic consequences of evolutionary shifts in body size, Ecology Letters, PDF 417 KB doi:10.1111/ele.12870

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.

Citation

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2017) Does the cost of development scale allometrically with offspring size?, Functional Ecology, PDF 943 KB doi:10.1111/1365-2435.13015

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.

Citation

Ghedini G, White CR, Marshall DJ (2017) Does energy flux predict density-dependence? An empirical field test. Ecology, PDF 380 KB doi:10.1002/ecy.2032

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.

Citation

Malerba ME, White C, Marshall DJ (2017) Phytoplankton size-scaling of net-energy flux across light and biomass gradients. Ecology, PDF 5.2 MB doi:10.1002/ecy.2032

Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects

Authors: Rolanda Lange and Dustin Marshall

Published in: Scientific Reports

Abstract

Stressors associated with global change will be experienced simultaneously and may act synergistically, so attempts to estimate the capacity of marine systems to cope with global change requires a multi-stressor approach.

Because recent evidence suggests that stressor effects can be context-dependent, estimates of how stressors are experienced in ecologically realistic settings will be particularly valuable.

To enhance our understanding of the interplay between environmental effects and the impact of multiple stressors from both natural and anthropogenic sources, we conducted a field experiment. We explored the impact of multiple, functionally varied stressors from both natural and anthropogenic sources experienced during early life history in a common sessile marine invertebrate, Bugula neritina.

Natural spatial environmental variation induced differences in conspecific densities, allowing us to test for density-driven context-dependence of stressor effects. We indeed found density-dependent effects. Under high conspecific density, individual survival increased, which offset part of the negative effects of experiencing stressors.

Experiencing multiple stressors early in life history translated to a decreased survival in the field, albeit the effects were not as drastic as we expected: our results are congruent with antagonistic stressor effects. We speculate that when individual stressors are more subtle, stressor synergies become less common.

Citation

Lange R, Marshall D (2017) Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Scientific reports, PDF 1 MB doi:10.1038/s41598-017-06373-y

Should mothers provision their offspring equally? A manipulative field test

Authors: Hayley Cameron, Keyne Monro, and Dustin J Marshall

Published in: Ecology Letters, volume 20, issue 8 (August 2017)

Abstract

Within-brood variation in offspring size is universal, but its causes are unclear. Theoretical explanations for within-brood variation commonly invoke bet-hedging, although alternatives consider the role of sibling competition. Despite abundant theory, empirical manipulations of within-brood variation in offspring size are rare.

Using a field experiment, we investigate the consequences of unequal maternal provisioning for both maternal and offspring fitness in a marine invertebrate. We create experimental broods of siblings with identical mean, but different variance, in offspring size, and different sibling densities.

Overall, more-variable broods had higher mean performance than less-variable broods, suggesting benefits of unequal provisioning that arise independently of bet-hedging. Complementarity effects drove these benefits, apparently because offspring-size variation promotes resource partitioning.

We suggest that when siblings compete for the same resources, and offspring size affects niche usage, the production of more-variable broods can provide greater fitness returns given the same maternal investment; a process unanticipated by the current theory.

Citation

Cameron H, Monro K, Marshall DJ (2017) Should mothers provision their offspring equally? A manipulative field test. Ecology Letters, PDF 799 KB  doi:10.1111/ele.12800

Do invasive species live faster? Mass-specific metabolic rate depends on growth form and invasion status

Authors: Marcelo E Lagos, Craig R White, and Dustin J Marshall

Published in: Functional Ecology

Abstract

Invasive organisms often share characteristics that make them successful. Traits such as rapid growth and short generation times are classic “weed” phenotypes, such that invasive species often have r-selected rather than k-selected life histories. Given that invasive species often display “fast” life histories, invasive species may have relatively higher metabolic rates but systematic tests across taxa are lacking.

We compared metabolic rate across 14 sessile invasive and native marine invertebrates. We also investigated the influence of growth form (erect vs. flat species) on the metabolic rate of these species, since growth form can also affect metabolic rate.

For species with an erect growth form, we found an effect of invasive status on mass-specific metabolic rate. Invasive species had much higher mass-specific metabolic rates than native species and this was particularly pronounced for organisms with smaller body masses.

Given that smaller-bodied invasive organisms are typically early-successional, “fugitive” species, a higher metabolic rate may allow a faster pace of life, enhancing their capacity to invade and reproduce in newly created disturbed habitats.

Citation

Lagos ME, White CR, Marshall DJ (2017) Do invasive species live faster? Mass-specific metabolic rate depends on growth form and invasion status. Functional Ecology, PDF 644 KB DOI:10.1111/1365-2435.12913

Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions

Authors: Marcelo E Lagos, Diego R Barneche, Craig R White, and Dustin J Marshall

Published in: Global Change Biology (early view)

Abstract

Biological invasions are one of the biggest threats to global biodiversity.

Marine artificial structures are proliferating worldwide and provide a haven for marine invasive species. Such structures disrupt local hydrodynamics, which can lead to the formation of oxygen-depleted microsites.

The extent to which native fauna can cope with such low oxygen conditions, and whether invasive species, long associated with artificial structures in flow-restricted habitats, have adapted to these conditions remains unclear.

We measured water flow and oxygen availability in marinas and piers at the scales relevant to sessile marine invertebrates (mm). We then measured the capacity of invasive and native marine invertebrates to maintain metabolic rates under decreasing levels of oxygen using standard laboratory assays.

We found that marinas reduce water flow relative to piers, and that local oxygen levels can be zero in low flow conditions. We also found that for species with erect growth forms, invasive species can tolerate much lower levels of oxygen relative to native species.

Integrating the field and laboratory data showed that up to 30% of available microhabitats within low flow environments are physiologically stressful for native species, while only 18% of the same habitat is physiologically stressful for invasive species.

These results suggest that invasive species have adapted to low oxygen habitats associated with manmade habitats, and artificial structures may be creating niche opportunities for invasive species.

Citation

Lagos ME, Barneche DR, White CR, Marshall DJ (2017) Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions. Global Change Biology PDF 1 MB doi:10.1111/gcb.13668