A global synthesis of offspring size variation, its eco‐evolutionary causes and consequences

Authors: Dustin J Marshall, Amanda K Pettersen, and Hayley Cameron

Published in: Functional Ecology, volume 32, issue 6 (June 2018)

Abstract

Offspring size is a key functional trait that can affect all phases of the life history, from birth to reproduction, and is common to all the Metazoa. Despite its ubiquity, reviews of this trait tend to be taxon‐specific. We explored the causes and consequences of offspring size variation across plants, invertebrates and vertebrates.

We find that offspring size shows clear latitudinal patterns among species: fish, amphibians, invertebrates and birds show a positive covariation in offspring size with latitude; plants and turtles show a negative covariation with latitude. We highlight the developmental window hypothesis as an explanation for why plants and turtles show negative covariance with latitude. Meanwhile, we find evidence for stronger, positive selection on offspring size at higher latitudes for most animals.

Offspring size also varies at all scales of organization, from populations through to broods from the same female. We explore the reasons for this variation and suspect that much of this variation is adaptive, but in many cases, there are too few tests to generalize.

We show that larger offspring lose relatively less energy during development to independence such that larger offspring may have greater net energy budgets than smaller offspring. Larger offspring therefore enter the independent phase with relatively more energy reserves than smaller offspring. This may explain why larger offspring tend to outperform smaller offspring but more work on how offspring size affects energy acquisition is needed.

While life‐history theorists have been fascinated by offspring size for over a century, key knowledge gaps remain. One important next step is to estimate the true energy costs of producing offspring of different sizes and numbers.

Citation

Marshall DJ, Pettersen AK, Cameron H (2018) A global synthesis of offspring size variation, its eco-evolutionary causes and consequences, Functional Ecology, PDF 792 KB doi:10.1111/1365-2435.13099

Testing MacArthur’s minimisation principle: do communities minimise energy wastage during succession?

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

Published in: Ecology Letters

Abstract

Robert MacArthur developed a theory of community assembly based on competition. By incorporating energy flow, MacArthur’s theory allows for predictions of community function. A key prediction is that communities minimise energy wastage over time, but this minimisation is a trade‐off between two conflicting processes: exploiting food resources, and maintaining low metabolism and mortality. Despite its simplicity and elegance, MacArthur’s principle has not been tested empirically despite having long fascinated theoreticians.

We used a combination of field chronosequence experiments and laboratory assays to estimate how the energy wastage of a community changes during succession. We found that older successional stages wasted more energy in maintenance, but there was no clear pattern in how communities of different age exploited food resources. We identify several reasons for why MacArthur’s original theory may need modification and new avenues to further explore community efficiency, an understudied component of ecosystem functioning.

Citation

Ghedini G, Loreau M, White CR, Marshall DJ (2018) Testing MacArthur’s minimisation principle: do communities minimise energy wastage during succession? Ecology Letters, PDF 350 KB, doi:10.1111/ele.13087

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

Metabolic scaling across succession: Do individual rates predict community‐level energy use?

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

Published in: Functional Ecology, volume 32, issue 6 (June 2018)

Abstract

A major goal of metabolic ecology is to make predictions across scales such that individual metabolic rates might be used to predict the metabolic rates of populations and communities, but the success of these predictions is unclear given the rarity of tests.

Given that older communities tend to have species with slower life histories and larger body sizes, we hypothesized that the metabolism of whole communities should scale allometrically with their mass across successional stages.

We created experimental chronosequences of sessile marine invertebrate communities in the field. We then:

  1. determined the metabolic scaling of these whole communities across successional stages of different mass, and
  2. tested whether the sum of individual metabolic rates for the dominant species could predict overall community metabolism.

Contrary to what we expected based on metabolic theory and succession theory, community metabolism scaled isometrically with mass across succession, despite the mean body size of dominant individuals within the communities increasing over time. We resolved this paradox by estimating community metabolism based on individual metabolic rates for the dominant species in the community. We show that non‐random changes in the membership of the species maintain mass‐specific metabolic rates of the whole community invariant across succession despite changes in size structure.

These results suggest that simple assumptions about how community‐level processes scale up from species are unlikely to be correct, because community turnover is non‐random with respect to metabolic rate. Nevertheless, with the appropriate parametrization, the sum of individual species rates can predict the function of the community as a whole.

Ghedini G, White CR, Marshall DJ (2018) Metabolic scaling across succession: Do individual rates predict community-level energy use?, Functional Ecology, PDF 909 KB doi:10.1111/1365-2435.13103

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