Fish reproductive-energy output increases disproportionately with body size

Authors: Diego R Barneche, D Ross Robertson, Craig R White, and Dustin J Marshall

Published in: Science, volume 360, issue 6389 (11 May 2018)

Abstract

Body size determines total reproductive-energy output.

Most theories assume reproductive output is a fixed proportion of size, with respect to mass, but formal macroecological tests are lacking. Management based on that assumption risks underestimating the contribution of larger mothers to replenishment, hindering sustainable harvesting.

We test this assumption in marine fishes with a phylogenetically controlled meta-analysis of the intraspecific mass scaling of reproductive-energy output.

We show that larger mothers reproduce disproportionately more than smaller mothers in not only fecundity but also total reproductive energy.

Our results reset much of the theory on how reproduction scales with size and suggest that larger mothers contribute disproportionately to population replenishment.

Global change and overharvesting cause fish sizes to decline; our results provide quantitative estimates of how these declines affect fisheries and ecosystem-level productivity.

Citation

Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish reproductive-energy output increases disproportionately with body size. Science. doi:10.1126/science.aao6868

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Cell size, photosynthesis and the package effect: an artificial selection approach

Authors: Martino E Malerba, Maria M Palacios, Yussi M, Palacios Delgado, John Beardall, and Dustin J Marshall

Published in: New Phytologist

Summary

Cell size correlates with most traits among phytoplankton species. Theory predicts that larger cells should show poorer photosynthetic performance, perhaps due to reduced intracellular self‐shading (i.e. package effect). Yet current theory relies heavily on interspecific correlational approaches and causal relationships between size and photosynthetic machinery have remained untested.

As a more direct test, we applied 250 generations of artificial selection (c. 20 months) to evolve the green microalga Dunaliella teriolecta (Chlorophyta) toward different mean cell sizes, while monitoring all major photosynthetic parameters.

Evolving larger sizes (>1500% difference in volume) resulted in reduced oxygen production per chlorophyll molecule – as predicted by the package effect. However, large‐evolved cells showed substantially higher rates of oxygen production – a finding unanticipated by current theory. In addition, volume‐specific photosynthetic pigments increased with size (Chla+b), while photo‐protectant pigments decreased (β‐carotene). Finally, larger cells displayed higher growth performances and Fv/Fm, steeper slopes of rapid light curves (α) and smaller light‐harvesting antennae (σPSII) with higher connectivity (ρ).

Overall, evolving a common ancestor into different sizes showed that the photosynthetic characteristics of a species coevolves with cell volume. Moreover, our experiment revealed a trade‐off between chlorophyll‐specific (decreasing with size) and volume‐specific (increasing with size) oxygen production in a cell.

Citation

Malerba ME, Palacios MM, Palacios Delgado YM, Beardall J, Marshall DJ (2018) Cell size, photosynthesis and the package effect: an artificial selection approach, New Phytologist, PDF 2 MB doi:10.1111/nph.15163

Biochemical evolution in response to intensive harvesting in algae: evolution of quality and quantity

Authors: Dustin J Marshall, Rebecca J Lawton, Keyne Monro, and Nicholas A Paul

Published in: Evolutionary Applications

Abstract

Evolutionary responses to indirect selection pressures imposed by intensive harvesting are increasingly common. While artificial selection has shown that biochemical components can show rapid and dramatic evolution, it remains unclear as to whether intensive harvesting can inadvertently induce changes in the biochemistry of harvested populations. For applications such as algal culture, many of the desirable bioproducts could evolve in response to harvesting, reducing cost‐effectiveness, but experimental tests are lacking.

We used an experimental evolution approach where we imposed heavy and light harvesting regimes on multiple lines of an alga of commercial interest for twelve cycles of harvesting and then placed all lines in a common garden regime for four cycles. We have previously shown that lines in a heavy harvesting regime evolve a “live fast” phenotype with higher growth rates relative to light harvesting regimes. Here, we show that algal biochemistry also shows evolutionary responses, although they were temporarily masked by differences in density under the different harvesting regimes. Heavy harvesting regimes, relative to light harvesting regimes, had reduced productivity of desirable bioproducts, particularly fatty acids.

We suggest that commercial operators wishing to maximize productivity of desirable bioproducts should maintain mother cultures, kept at higher densities (which tend to select for desirable phenotypes), and periodically restart their intensively harvested cultures to minimize the negative consequences of biochemical evolution.

Our study shows that the burgeoning algal culture industry should pay careful attention to the role of evolution in intensively harvested crops as these effects are nontrivial if subtle.

Marshall DJ, Lawton RJ, Monro K, Paul NA (2018) Biochemical evolution in response to intensive harvesting in algae: evolution of quality and quantity. Evolutionary Applications, PDF 746 KB doi:10.1111/eva.12632

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

Genotypic covariance between the performance of a resident species and community assembly in the field

Authors: Arthur M Riedel, Keyne Monro, Mark W Blows, and Dustin J Marshall

Published in: Functional Ecology, volume 32, issue 2 (February 2018)

Abstract

Genetic variation in resident species can influence the assembly and dynamics of communities, but the potential for these genetic effects to persist across generations is largely unresolved. In principle, persistent, directional changes in communities are only predicted when community properties covary genetically with the fitness of resident species.

Estimates of genetic covariance between the fitness of a resident species and its community are therefore necessary to “close the eco-evolutionary loop” in studies of community genetics, but such estimates are rare. Emulating community genetics experiments in plants, we used clonal replicates of 21 genotypes of a resident species (the encrusting bryozoan, Hippopodina) to investigate the magnitude of genotypic variance contributing to assembly of a marine benthic community.

Genotypes explained up to 35% of variation in community assembly. Critically, the performance of Hippopodina genotypes covaried both with the evenness of communities and with the abundances of some individual species, representing an indirect genetic effect that creates the potential for multigenerational interactions between Hippopodina and co-existing species. Our results suggest that different genotypes will associate with different community members consistently across generations, and such non-random associations can give rise to specialization. Further interactions between species other than Hippopodina itself may also be altered by effects of genetic variation in the focal species.

Furthermore, species in the community other than Hippopodina itself will interact more commonly in the presence of some genotypes over others.

Our results support the potential for genetic variation in one species to have deterministic effects on the dynamics of ecological communities.

Citation

Riedel AM, Monro K, Blows MW, Marshall DJ (2018) Genotypic covariance between the performance of a resident species and community assembly in the field, Functional Ecology, PDF 945 KB doi:/10.1111/1365-2435.13005

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 874 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