Metabolism drives demography in an experimental field test

Authors: Lukas Schuster, Hayley Cameron, Craig R White, and Dustin J Marshall

Published in: Proceedings of the National Academy of Sciences of the United States of America

Significance

Biology has long-standing rules about how metabolism and demography should covary. These rules connect physiology to ecology but remarkably, these rules have only ever been tested indirectly.

Using a model marine invertebrate, we created experimental field populations that varied in metabolic rate but not body size.

We show that metabolism qualitatively affects population growth and carrying capacity in ways predicted by theory but that scaling relationships for these parameters, as well as estimates of energy use at carrying capacity, depart from classic predictions.

That metabolism affects demography in ways that depart from canonical theory has important implications for predicting how populations may respond to global change and size-selective harvesting.

Abstract

Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing “rules” for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries.
Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare.

In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment.

We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory—in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence.

Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.

Schuster L, Cameron H, White CR, Marshall DJ (2021) Metabolism drives demography in an experimental field test. Proceedings of the National Academy of Sciences of the United States of America DOI

Reproductive hyperallometry and managing the world’s fisheries

Authors: Dustin J Marshall, Michael Bode, Marc Mangel, Robert Arlinghaus, and EJ Dick

Published in: Proceedings of the National Academy of Sciences of the United States of America

Significance

We find that a ubiquitous assumption in fisheries models for predicting population replenishment introduces systematic overestimates of replenishment in fished populations.

For 32 of the world’s major fisheries, these biases result in harvest thresholds being set too high: in most cases, reference points based on spawning potential ratios are more than 2.5 times higher than those necessary to achieve the desired level of replenishment.

When we use the more biologically appropriate assumption of reproductive hyperallometry, we find that management tools such as spatiotemporal closures and harvest slots can outperform traditional approaches in terms of yield.

Failing to consider reproductive hyperallometry overestimates the efficacy of traditional fisheries management and underestimates the benefits of approaches that create reservoirs of larger individuals.

Abstract

Marine fisheries are an essential component of global food security, but many are close to their limits and some are overfished. The models that guide the management of these fisheries almost always assume reproduction is proportional to mass (isometry), when fecundity generally increases disproportionately to mass (hyperallometry).

Judged against several management reference points, we show that assuming isometry overestimates the replenishment potential of exploited fish stocks by 22% (range: 2% to 78%) for 32 of the world’s largest fisheries, risking systematic overharvesting.

We calculate that target catches based on assumptions of isometry are more than double those based on assumptions of hyperallometry for most species, such that common reference points are set twice as high as they should be to maintain the target level of replenishment.

We also show that hyperallometric reproduction provides opportunities for increasing the efficacy of tools that are underused in standard fisheries management, such as protected areas or harvest slot limits. Adopting management strategies that conserve large, hyperfecund fish may, in some instances, result in higher yields relative to traditional approaches.

We recommend that future assessment of reference points and quotas include reproductive hyperallometry unless there is clear evidence that it does not occur in that species.

Marshall DJ, Bode M, Mangel M, Arlinghaus R, Dick EJ (2021) Reproductive hyperallometry and managing the world’s fisheries. Proceedings of the National Academy of Sciences of the United States of America DOI

Effects of light variation in algal cultures: a systematic map of temporal scales

Authors: Belinda Comerford, Nicholas Paul, and Dustin J Marshall

Published in: Journal of Applied Phycology

Abstract

Algal aquaculture is a rapidly growing field, with a proliferation of studies exploring algal growth. The expansion of the field not only presents opportunities for synthesis, but also creates challenges in identifying where the strengths and knowledge gaps exist.

One tool for formally quantifying the state of knowledge is a systematic map, already useful in many fields, but underutilised in algal research. We used a systematic map to describe variable light regimes in algal cultures.

Light variation is ubiquitous in algal cultures and spans a range of temporal scales (microseconds to months), but it is unclear which scales have been explored.

We characterised 1393 experiments according to the temporal scale of light variation that was manipulated. Intensely studied light variation frequencies were either very short (< seconds) or long (diel cycles); the prominent gap was frequencies between these extremes (seconds to hours), especially for experiments that lasted for long durations (> months). Experiments that lasted for days were most common, while few studies lasted for months or more. Most studies were conducted in small culture vessels, used instantaneous changes in light regimes, and few studies reported initial stocking density metrics consistently.

Our map highlights that the field has accumulated a rich knowledge base that is ripe for synthesis in some areas, particularly very short or relatively long frequency light variation. The map indicates that the key priorities are explorations of intermediate frequencies and our understanding of their effects is limited. Similarly, our understanding of evolutionary responses to variable light regimes of all scales is lagging.

Comerford B, Paul N, Marshall D (2021) Effects of light variation in algal cultures: a systematic map of temporal scales. Journal of Applied Phycology PDF DOI

Temperature-mediated variation in selection on offspring size: A multi-cohort field study

Author: Dustin J Marshall

Published in: Functional Ecology

Abstract

Offspring size is a key life-history trait that often covaries negatively with temperature. Most studies focus on how temperature alters selection on offspring size during early life-history stages such as embryos or larvae. The degree to which temperature alters the relationship between offspring size and post-metamorphic performance remains unclear as field studies across multiple temperature regimes are rare.

I deployed over 6,000 individuals of known offspring size, into the field across 28 cohorts spanning 4 years for the model marine invertebrate, Bugula neritina and monitored their survival, growth and reproduction.

Offspring size closely tracked the local environmental temperature across cohorts. This offspring size–temperature covariance appeared to be adaptive, at least from the perspective of mothers. When temperatures were warmer, the relationship between offspring size and performance was weak; when temperatures were cooler, the relationship was strongly positive.

The estimates of selection based on maternal fitness differed from those based on offspring fitness, suggesting temperature-mediated parent–offspring conflict over offspring provisioning exists. I also found evidence for temporal autocorrelation in temperature and selection on offspring size.

The fact that temperature affects the relationship between offspring size and post-metamorphic performance further complicates the challenge in understanding the ubiquitous covariance between offspring size and temperature.

Marshall DJ (2021) Temperature‐mediated variation in selection on offspring size: A multi‐cohort field study. Functional Ecology PDF DOI

Larger cells have relatively smaller nuclei across the Tree of Life

Authors: Martino E Malerba and Dustin J Marshall

Published in: Evolution Letters

Abstract

Larger cells have larger nuclei, but the precise relationship between cell size and nucleus size remains unclear, and the evolutionary forces that shape this relationship are debated.

We compiled data for almost 900 species – from yeast to mammals – at three scales of biological organisation: among-species, within-species, and among-lineages of a species that was artificially selected for cell size.

At all scales, we showed that the ratio of nucleus size to cell size (the ‘N: C’ ratio) decreased systematically in larger cells. Size evolution appears more constrained in nuclei than cells: cell size spans across six orders of magnitude, whereas nucleus size varies by only three.

The next important challenge is to determine the drivers of this apparently ubiquitous relationship in N:C ratios across such a diverse array of organisms.

Malerba ME, Marshall DJ (2021) Larger cells have relatively smaller nuclei across the Tree of Life. Evolution Letters PDF DOI

Geographical bias in physiological data limits predictions of global change impacts

Authors: Craig R White, Dustin J Marshall, Steven L Chown, Susana Clusella‐Trullas, Steven J Portugal, Craig E Franklin and Frank Seebacher

Published in: Functional Ecology

Abstract

Climate affects all aspects of biology. Physiological traits play a key role in mediating these effects, because they define the fundamental niche of each organism.

Climate change is likely to shift environmental conditions away from physiological optima. The consequences for species are significant: they must alter their physiology through plasticity or adaptation, move, or decline to extinction. The ability to understand and predict such organismal responses to global change is, however, only as good as the geographical coverage of the data on which these predictions are based.

Geographical biases in the state of physiological knowledge have been identified, but it has not been determined if these geographical biases are likely to limit our capacity to predict the outcomes of global change. We show that current knowledge of physiological traits is representative of only a limited range of the climates in which terrestrial animals will be required to operate, because data for animals from only a limited range of global climates have been incorporated in existing compilations.

We conclude that geographical bias in existing datasets limits our capacity to predict organismal responses in the vast areas of the planet that are unstudied, and that this geographical bias is a much greater source of uncertainty than the difference between the current climate and the projected future climate. Addressing this bias is urgent to understand where impacts will be most profound, and where the need for intervention is most pressing.

White CR, Marshall DJ, Chown SL, Clusella‐Trullas S, Portugal SJ, Franklin CE, Seebacher F (2021) Geographical bias in physiological data limits predictions of global change impacts. Functional Ecology PDF DOI

Plastic but not adaptive: habitat‐driven differences in metabolic rate despite no differences in selection between habitats

Authors: Lukas Schuster, Craig R White, and Dustin J Marshall

Published in: Oikos

Abstract

Metabolic plasticity in response to different environmental conditions is widespread across taxa. It is reasonable to expect that such plasticity should be adaptive, but only few studies have determined the adaptive significance of metabolic plasticity by formally estimating selection on metabolic rate under different environmental conditions.

We used a model marine colonial invertebrate, Bugula neritina to examine selection on metabolic rate in a harsh and a benign environment in the field, then tested whether these environments induced the expression of different metabolic phenotypes. We conducted two experimental runs and found evidence for positive correlational selection on the combination of metabolic rate and colony size in both environments in one run, whereas we could not detect any selection on metabolic rate in the second run.

Even though there was no evidence for different selection regimes in the different environments, colonies expressed different metabolic phenotypes depending on the environment they experienced. Furthermore, there was no relationship between the degree of plasticity expressed by an individual and their subsequent fitness.

In other words, we found evidence for phenotypic plasticity in metabolic rate, but there was no evidence that this plasticity was adaptive. In the absence of estimates of performance, changes in metabolic rate should not be assumed to be adaptive.

Schuster L, White CR, Marshall DJ (2021) Plastic but not adaptive: habitat‐driven differences in metabolic rate despite no differences in selection between habitats. Oikos PDF DOI

Multilevel selection on offspring size and the maintenance of variation

Authors: Hayley Cameron, Darren W Johnson, Keyne Monro, and Dustin J Marshall

Published in: The American Naturalist

Abstract

Multilevel selection on offspring size occurs when offspring fitness depends on both absolute size (hard selection) and size relative to neighbors (soft selection).

We examined multilevel selection on egg size at two biological scales — within clutches and among clutches from different females — using an external fertilizing tube worm. We exposed clutches of eggs to two sperm environments (limiting and saturating) and measured their fertilization success. We then modeled environmental (sperm-dependent) differences in hard and soft selection on individual eggs as well as selection on clutch-level traits (means and variances).

Hard and soft selection differed in strength and form depending on sperm availability—hard selection was consistently stabilizing; soft selection was directional and favored eggs relatively larger (sperm limitation) or smaller (sperm saturation) than the clutch mean. At the clutch level, selection on mean egg size was largely concave, while selection on within-clutch variance was weak but generally negative—although some correlational selection occurred between these two traits. Importantly, we found that the optimal clutch mean egg size differed for mothers and offspring, suggesting some antagonism between the levels of selection.

We thus identify several pathways that may maintain offspring size variation: environmentally (sperm-) dependent soft selection, antagonistic multilevel selection, and correlational selection on clutch means and variances.

Multilevel approaches are powerful but seldom-used tools for studies of offspring size, and we encourage their future use.

Cameron H, Johnson DW, Monro K, Marshall DJ (2021) Multilevel selection on offspring size and the maintenance of variation. The American Naturalist PDF DOI

Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Authors: Martino E Malerba, Dustin J Marshall, Maria M Palacios, John A Raven, and John Beardall

Published in: New Phytologist

Summary

Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume‐specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2‐concentrating mechanisms (CCMs).

Previous studies have focused on among‐species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3‐fold difference in cell volume. We compared CO2affinity, external carbonic anhydrase (CAext), isotopic signatures (δ13C) and growth among size‐selected lineages.

Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13C. Larger cells also achieved faster growth and higher maximum biovolume densities.

We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

Malerba ME, Marshall DJ, Palacios MM, Raven JA, Beardall J (2020) Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New Phytologist PDF DOI

Projecting marine developmental diversity and connectivity in future oceans

Authors: Dustin J Marshall and Mariana Álvarez-Noriega

Published in: Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Global change will alter the distribution of organisms around the planet. While many studies have explored how different species, groups and traits might be re-arranged, few have explored how dispersal is likely to change under future conditions.

Dispersal drives ecological and evolutionary dynamics of populations, determining resilience, persistence and spread. In marine systems, dispersal shows clear biogeographical patterns and is extremely dependent on temperature, so simple projections can be made regarding how dispersal potentials are likely to change owing to global warming under future thermal regimes.

We use two proxies for dispersal — developmental mode and developmental duration. Species with a larval phase are more dispersive than those that lack a larval phase, and species that spend longer developing in the plankton are more dispersive than those that spend less time in the plankton.

Here, we explore how the distribution of different development modes is likely to change based on current distributions. Next, we estimate how the temperature-dependence of development itself depends on the temperature in which the species lives, and use this estimate to project how developmental durations are likely to change in the future.

We find that species with feeding larvae are likely to become more prevalent, extending their distribution poleward at the expense of species with aplanktonic development. We predict that developmental durations are likely to decrease, particularly in high latitudes where durations may decline by more than 90%. Overall, we anticipate significant changes to dispersal in marine environments, with species in the polar seas experiencing the greatest change.

This article is part of the theme issue ‘Integrative research perspectives on marine conservation’.

Marshall DJ, Álvarez-Noriega M (2020) Projecting marine developmental diversity and connectivity in future oceans. Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI