Authors: Dustin Marshall, Craig R White, Van Savage, and Naomi Levine

Published in: Trends in Ecology & Evolution

Highlights

First-principles approaches underpin many biological theories, many of which claim to be firmly grounded in physics, such that their principles are inviolable.

Many predictions about how global change will affect biological systems are based on biological theories that purport to be based on first principles.

Many first-principles approaches are based on incomplete physics, while others have surprising biological assumptions at their core that are often overlooked.

We argue that first-principles approaches in biology can be powerful and hold tremendous promise, but biologists should increase their scrutiny of these approaches.

Abstract

First-principles approaches, based on physics or chemistry, are key pillars of biological theory. Despite their value, there are recurrent problems with many first-principles approaches in biology: they often include incomplete physics or are driven by unscrutinised biological assumptions. Meanwhile, debates about biological theories based on first principles usually focus on the fit of predictions to data—we argue such a focus confuses prediction with explanation.

A good fit of predictions to data is a necessary, but insufficient condition for a theory to be sound. First-principles approaches in biology will only be effective when the physics and biology are both sufficiently complete. Determining what elements are essential to include is an enduring but exciting challenge of science.

Marshall D, White CR, Savage V, Levine N (2026) Second thoughts about first principles in biology. Trends in Ecology & Evolution PDF DOI

Authors: Dustin J Marshall, Hayley E Cameron, Akira Abe, Suzana Goncalves Leles, Craig R White, and John DeLong

Published in: Ecology Letters

Abstract

The communities of unicellular microbes (bacteria, protists and yeasts) that underpin ecosystems are changing. In warmer conditions, protists tend to shrink, but the consequences of these changes in size are unclear. We show preliminary evidence that warming-mediated declines in cell size observed in protists also apply to bacteria and yeasts.

Predicting the consequences of these warming-mediated size declines requires that the relationships between cell size and key functional traits are well-characterised. We show that the critical relationship between unicellular size and energy use—that is, metabolic scaling—has been systematically mis-estimated in the past. Projections of the effects of warming on unicellular respiration change from superlinear to sublinear once the metabolic scaling relationship is updated, with worrying consequences for the biological carbon pump and other ecosystem services. Other size-function scaling relationships (e.g., photosynthesis) are likely to have been similarly mis-estimated.

Next, we show that theory on the relationships between size, temperature and demography is more ambivalent than previously recognised, leaving uncertainty as to how warming will alter the dynamics of unicellular populations.

Finally, we identify pathways for improving our capacity to predict future changes in unicellular size, and decrease the uncertainty surrounding the consequences of these changes.

Marshall DJ, Cameron HE, Abe A, Leles SG, White CR, DeLong J (2026) Drivers and consequences of size declines in unicells. Ecology Letters PDF DOI

Authors: Jan Kozłowski, Dustin J Marshall, and Craig R White

Published in: Science

Editor’s summary

Anthropogenic climate change is altering environments. Species do respond to such changes, but how quickly this can happen remains unknown. Fish have been shown to evolve rapidly in response to changing conditions, but outcomes are difficult to predict.

Kozłowski et al. modeled the selective adaptation to warming waters and predicted that fish in these waters will grow faster but will also mature to smaller sizes (see the Perspective by Travis and Reznick).

Although the authors concluded that this will help fish survive warming conditions, it will also decrease fisheries yields, with the greatest decreases under the most extreme conditions.

Failing to integrate adaptation in fisheries models greatly overestimates yields, leading to reduced sustainability.

— Sacha Vignieri

Abstract

Global warming is altering the fisheries that underpin food security, but projections of these impacts generally exclude evolutionary processes.

We describe a model that forecasts how fish will adapt to future climates and the consequences of that evolution for fisheries yields.

We predict that fish in warmer waters will grow faster but evolve earlier maturation, decreasing their maximum size. We predict that evolution ameliorates the impacts of climate change on fish fitness but exacerbates its impacts on fisheries yields — worsening losses by ~50%.

Excluding evolution overestimates future yields under all emissions scenarios, but evolution’s impacts are greatest under the most extreme scenarios. All life histories may evolve in response to global change — this evolution should be considered in projections of ecosystems and their services.

Kozłowski J, Marshall DJ, White CR (2026) Evolutionary adaptation to global change reduces sustainable fisheries yields. Science DOI

Authors: George C Jarvis and Dustin J. Marshall

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Hermaphroditism, where an individual can reproduce as both male and female, offers some clear reproductive advantages. Simultaneous hermaphroditism guarantees that every mature adult can mate with another—a particular advantage when opportunities to mate are scarce.

Despite this potential benefit, hermaphroditism is relatively rare in animals.

This paradox has long involved an energetics argument: hermaphrodites require more energy to fuel two reproductive roles instead of only one, which favours the evolution of separate sexes. However, this argument has never been tested.

Here, we compare resting metabolic rates between hermaphrodites and gonochores across 536 species of marine invertebrates, spanning 11 phyla.

Our analyses, which control for body size, environmental temperature, motility and phylogeny, contradict predictions from classic theory: instead of requiring more energy than gonochores, hermaphrodites require approximately 27% less energy on average.

These findings overturn a 150-year-old argument that hermaphroditism is rarer in animals because it is more costly and highlight the need to reconsider the role of energetics in the evolution of sexual systems.

Jarvis GC, Marshall DJ (2025) Hermaphrodites have lower metabolic rates than gonochores. Proceedings of the Royal Society B: Biological Sciences PDF DOI

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

Published in: Journal of Applied Phycology

Abstract

Humans modify the habitats of cultured species to maximise productivity, creating conditions distinct from those in which those species originally evolved. These human-altered environments impose strong selection pressures that favour novel phenotypes. While instances of deliberate selection for favoured phenotypes are ubiquitous, the consequences of unintentional selection regimes associated with culture conditions are less well understood.

With their high stocking densities and circulating nature, land-based seaweed cultures are likely to generate light regimes that are vastly different from those of the natural environment, but explicit tests are lacking.

Here, we quantified how light environments experienced by seaweed in land-based culture tanks differ from those of the natural environment.

We found significant differences in culture and natural light environments. Cultures were usually much darker, but occasionally much brighter and the light regimes were less predictable than those occurring in the natural environment.

Our results highlight that in our system, land-based seaweed cultures generated light regimes unlike anything in nature and this likely presents challenges for seaweed adaptation and scaling up of production.

Comerford B, Paul NA, Marshall DJ (2025) Land-based seaweed cultivation creates darker, less predictable light environments. Journal of Applied Phycology PDF DOI

Authors: Samuel C Ginther, Hayley Cameron, Craig R White, and Dustin G Marshall

Published in: Science

Abstract

Reproduction includes two energy investments — the energy in the offspring and the energy expended to make them. The former is well understood, whereas the latter is unquantified but often assumed to be small. Without understanding both investments, the true energy costs of reproduction are unknown.

We present a framework for estimating the total energy costs of reproduction by combining data on the energy content of offspring (direct costs) and the metabolic load of bearing them (indirect costs).

We find that direct costs typically represent the smaller fraction of the energy expended on reproduction. Mammals pay the highest reproductive costs (excluding lactation), ~90% of which are indirect. Ectotherms expend less on reproduction overall, and live-bearing ectotherms pay higher indirect costs compared with egg-layers. We show that the energy demands of reproduction exceed standard assumptions.

Ginther SC, Cameron H, White CR, Marshall DJ (2024) Metabolic loads and the costs of metazoan reproduction. Science PDF DOI

Author: Dustin J Marshall

Published in: Ecology Letters

Abstract

Good experimental design is critical for sound empirical ecology and evolution. However, many contemporary studies fail to replicate at the appropriate biological or organizational level, so causal inference might have less vigorous support than often assumed.

Here, I provide a guide for how to identify the appropriate scale of replication for a range of common experimental designs in ecological and evolutionary studies. I discuss the merits of replicating multiple scales of biological organization. I suggest that experimental design be discussed in terms of the scale of replication relative to the scale at which inferences are sought when designing, discussing and reviewing experiments in ecology and evolution.

I also suggest that more conversations about experimental design are needed, and I hope this piece stimulates such conversation.

Marshall DJ (2024) Principles of experimental design for ecology and evolution. Ecology Letters PDF DOI 

Authors: Ashley E Potter, Craig R White and Dustin J Marshall

Published in: Journal of Experimental Biology

Abstract

From bacteria to metazoans, higher density populations have lower per capita metabolic rates than lower density populations. The negative covariance between population density and metabolic rate is thought to represent a form of adaptive metabolic plasticity. A relationship between density and metabolism was actually first noted 100 years ago, and was focused on spermatozoa; even then, it was postulated that adaptive plasticity drove this pattern. Since then, contemporary studies of sperm metabolism specifically assume that sperm concentration has no effect on metabolism and that sperm metabolic rates show no adaptive plasticity.

We did a systematic review to estimate the relationship between sperm aerobic metabolism and sperm concentration, for 198 estimates spanning 49 species, from protostomes to humans from 88 studies.

We found strong evidence that per capita metabolic rates are concentration dependent: both within and among species, sperm have lower metabolisms in dense ejaculates, but increase their metabolism when diluted. On average, a 10-fold decrease in sperm concentration increased per capita metabolic rate by 35%. Metabolic plasticity in sperm appears to be an adaptive response, whereby sperm maximize their chances of encountering eggs.

Potter AE, White CR, Marshall DJ (2024) Per capita sperm metabolism is density dependent. Journal of Experimental Biology PDF DOI 

Authors: Matthew D Hall, Ben L Phillips, Craig R White, and Dustin J. Marshall

Published in: Functional Ecology

Abstract

Exposure to a pathogen is predicted to lead to increased energy use as hosts attempt to activate a costly immune system and repair damaged tissue. To meet this demand, metabolic rates, which capture the rate at which a host can use, transform and expend energy, are expected to increase. Yet for many host–pathogen systems, metabolic rates after encountering a pathogen are just as likely to decrease as increase, suggesting that increased energy expenditure may not always be best for fighting infection.

Diverging metabolic trajectories have been previously attributed to the different pathways that specific pathogen classes, such as bacteria or viruses, induce in a host. Here, we test how the magnitude and direction of metabolic change following pathogen exposure might also depend on whether a host has cleared infection or is instead fighting to reduce pathogen burden, as well as interactions between host and pathogen genotypes of a single host–pathogen system.

Using a model system, Daphnia magna and its bacterial pathogen, we quantified changes in mass-independent metabolic rates over a 30-day period for multiple host and pathogen genotypes. We found that the metabolic trajectory of an exposed host diverged quickly during the infection process. For hosts that were exposed to a pathogen and resisted infection, their mass-independent metabolic rates remained suppressed long after exposure, leading to a sustained reduction in total energy use compared to unexposed animals. The reverse was true for hosts in which the pathogen was able to establish an infection.

Underlying these changes were differences in the energetic burden that each pathogen genotype imposed on its host, as well as changes in the way host genotype and the outcome of infection shaped underlying scaling relationships between host body mass and metabolic rates. Our results demonstrate how variation in an organism’s  metabolic rate and overall energy use can arise from within a single host–pathogen encounter and depend on the likelihood of pathogen clearance, as well as the within-species genetic variability of both hosts and pathogens.

Hall MD, Phillips BL, White CR, Marshall DJ (2024) The hidden costs of resistance: Contrasting the energetics of successfully and unsuccessfully fighting infection. Functional Ecology PDF DOI 

Authors: Hayley Cameron and Dustin Marshall

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

Abstract

As physiologists seek to better understand how and why metabolism varies, they have focused on how metabolic rate covaries with fitness—that is, selection.

Evolutionary biologists have developed a sophisticated framework for exploring selection, but there are particular challenges associated with estimating selection on metabolic rate owing to its allometric relationship with body mass. Most researchers estimate selection on mass and absolute metabolic rate; or selection on mass and mass-independent metabolic rate (MIMR)—the residuals generated from a nonlinear regression. These approaches are sometimes treated as synonymous: their coefficients are often interpreted in the same way.

Here, we show that these approaches are not equivalent because absolute metabolic rate and MIMR are different traits. We also show that it is difficult to make sound biological inferences about selection on absolute metabolic rate because its causal relationship with mass is enigmatic. By contrast, MIMR requires less-desirable statistical practices (i.e. residuals as a predictor), but provides clearer causal pathways. Moreover, we argue that estimates of selection on MIMR have more meaningful interpretations for physiologists interested in the drivers of variation in metabolic allometry.

Cameron H, Marshall D (2024) Estimating the relationship between fitness and metabolic rate: which rate should we use? Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI