How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J Marshall, Carla M Sgrò, and Keyne Monro

Published in: Proceedings of the Royal Society B

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change?, Proceedings of the Royal Society B, PDF 556 KB doi:10.1098/rspb.2018.1374

Global environmental drivers of marine fish egg size

Authors: Diego R Barneche, Scott C Burgess, and Dustin J Marshall

Published in: Global Ecology and Biogeography, volume 27, issue 8 (August 2018)

Abstract

Aim: To test long‐standing theory on the role of environmental conditions (both mean and predictability) in shaping global patterns in the egg sizes of marine fishes.

Location: Global (50° S to 50° N).

Time period: 1880 to 2015.

Major taxa studied: Marine fish.

Methods: We compiled the largest geo‐located dataset of marine fish egg size (diameter) to date (n = 1,078 observations; 192 studies; 288 species; 242 localities). We decomposed sea surface temperature (SST) and chlorophyll‐a time series into mean and predictability (seasonality and colour of environmental noise – i.e. how predictable the environment is between consecutive time steps), and used these as predictors of egg size in a Bayesian phylogenetic hierarchical model. We test four specific hypotheses based on the classic discussion by Rass (1941), as well as contemporary life‐history theory, and the conceptual model of Winemiller and Rose (1992).

Results: Both environmental mean and predictability correlated with egg size. Our parsimonious model indicated that egg size decreases by c. 2.0‐fold moving from 1 to 30 °C. Environments that were more seasonal with respect to temperature were associated with larger eggs. Increasing mean chlorophyll‐a, from 0.1 to 1 mg/m3, was associated with a c. 1.3‐fold decrease in egg size. Lower chlorophyll‐a seasonality and reddened noise were also associated with larger egg sizes – aseasonal but more temporally autocorrelated resource regimes favoured larger eggs.

Main conclusions: Our findings support results from Rass (1941) and some predictions from Winemiller and Rose (1992). The effects of environmental means and predictability on marine fish egg size are largely consistent with those observed in marine invertebrates with feeding larvae, suggesting that there are important commonalities in how ectotherm egg size responds to environmental change. Our results further suggest that anthropogenically mediated changes in the environment will have profound effects on the distribution of marine life histories.

Citation

Barneche DR, Burgess SC, Marshall DJ (2018) Global environmental drivers of marine fish egg size, Global Ecology and Biogeography, PDF 9 MB doi:10.1111/geb.12748

Resources mediate selection on module longevity in the field

Authors: Karin Svanfeldt, Keyne Monro, and Dustin J Marshall

Published in: Evolutionary Biology

Abstract

The life histories of modular organisms are complicated, where selection and optimization can occur at both organismal and modular levels.

At a modular level, growth, reproduction and death can occur in one module, independently of others. Across modular groups, there are no formal investigations of selection on module longevity.

We used two field experiments to test whether selection acts on module longevity in a sessile marine invertebrate and whether selection varies across successional gradients and resource regimes.

We found that selection does act on module longevity and that the strength of selection varies with environmental conditions. In environments where interspecific competition is high, selection favours colonies with longer zooid (module) longevity for colonies that initially received high levels of maternal investment. In environments where food availability is high and flow rate is low, selection also favours colonies with longer zooid longevity.

These patterns of selection provide partial support for module longevity theory developed for plants. Nevertheless, that selection on module longevity is so context‐dependent suggests that variation in module longevity is likely to be maintained in this system.

Citation

Svanfeldt K, Monro K, Marshall DJ (2018) Resources mediate selection on module longevity in the field, Journal of Evolutionary Biology, PDF 350 KB doi:10.1111/jeb.13362

Do larger individuals cope with resource fluctuations better? An artificial selection approach

Authors: Martino E Malerba, Maria M Palacios, and Dustin J Marshall

Published in: Proceedings of the Royal Society B

Abstract

Size determines the rate at which organisms acquire and use resources but it is unclear what size should be favoured under unpredictable resource regimes.

Some theories claim smaller organisms can grow faster following a resource pulse, whereas others argue larger species can accumulate more resources and maintain growth for longer periods between resource pulses. Testing these theories has relied on interspecific comparisons, which tend to confound body size with other life-history traits.

As a more direct approach, we used 280 generations of artificial selection to evolve a 10-fold difference in mean body size between small- and large-selected phytoplankton lineages of Dunaliella tertiolecta, while controlling for biotic and abiotic variables. We then quantified how body size affected the ability of this species to grow at nutrient-replete conditions and following periods of nitrogen or phosphorous deprivation.

Overall, smaller cells showed slower growth, lower storage capacity and poorer recovery from phosphorous depletion, as predicted by the ‘fasting endurance hypothesis’. However, recovery from nitrogen limitation was independent of size—a finding unanticipated by current theories.

Phytoplankton species are responsible for much of the global carbon fixation and projected trends of cell size decline could reduce primary productivity by lowering the ability of a cell to store resources.

Citation

Malerba ME, Palacios MM, Marshall DJ (2018) Do larger individuals cope with resource fluctuations better? An artificial selection approach, Proceedings of the Royal Society B, PDF 2 MB doi:10.1098/rspb.2018.1347

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