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.

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 DOI 

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

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.

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 DOI 

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

20 years after ‘View from the Park’: advance ecology and avoid editorial rejection in Oikos

Authors: Dries Brote, Dustin J Marshall, Gerlinde B De Deyn, and Pedro R Peres-Neto

Published in: Oikos

Oikos has a long-standing tradition in publishing original and innovative research on all aspects of ecology. The journal’s emphasis has always been on theoretical and empirical work aimed at generalization and synthesis across taxa, systems and ecological disciplines. At the same time, Oikos has always been a little quirky – a little odder than other, equally valuable ecologically focused journals. This balance of quirkiness and rigour was best captured but John Lawton’s View from the park contributions that influenced our thinking and practice in ecology. The “View from the Park” essays remain timely and relevant; Lawton presciently communicated key concerns about ecological research that continue to resonate 20 years later:

  • the disparate and uncoordinated study of processes and patterns across too many haphazardly chosen model species,
  • the lack of a proper theoretical basis in many ecological studies,
  • mismatches between experimental and natural scales, and
  • the overestimation of ecological relevance of the researchers’ own pet species.

(continues…)

Bonte D, Marshall D, De Deyn GB, Peres-Neto PR (2018) 20 years after View from the Park: advance ecology and avoid editorial rejection in Oikos, 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