Authors: Will Morgan, Hayley E Cameron and Dustin J Marshall

Published in: Evolution Letters

Abstract

Theory predicts that aged-related declines in performance (senescence) depend on experiences during early life. Experimental field tests of this theory are rare: most manipulative studies have been done in the laboratory on short-lived invertebrates; while most field studies focus on longer-lived vertebrates and involve no experimental manipulation. Consequently, few studies manipulate early-life stress and test its effects on senescence in the field, especially in invertebrates.

We manipulated early-life stress in the colonial marine bryozoan, Bugula neritina, by experimentally extending the larval period (an energetic stress), then monitored the survival, fecundity and growth of more than 500 individuals in the field across their lifetimes. We used these data to generate trajectories of actuarial and reproductive senescence and test how both components of ageing were affected by early-life stress.

While colonial organisms with indeterminate growth such as B. neritina have been theorised to show negligible senescence, instead we saw strong declines in survival and reproductive output in the oldest individuals, regardless of early-life stress. We also found that adults originating from stressed larvae had lower fitness overall (in terms of lifetime reproductive success), but experienced weaker actuarial senescence.

Our findings for reproductive senescence were more nuanced, with some evidence to suggest that early-life stress also decreases rates of reproductive senescence. Our study provides a rare demonstration of senescence for an invertebrate in the field and suggests that the relationship between life history and senescence may be more complex than has been anticipated.

Morgan W, Cameron HE, Marshall DJ (2026) Early-life stress reduces senescence in the field for an indeterminately growing ectotherm. Evolution Letters PDF DOI

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 PDF 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: Heverton LC Dutra, Dustin J Marshall, Belinda Comerford, Brianna P McNulty, Anastacia M Diaz, Matthew J Jones, Austin J Mejia, Ottar N Bjornstad, and Elizabeth A McGraw

Published in: PLOS Neglected Tropical Diseases

Abstract

Background Climate change and urbanization will alter the global distribution of disease vectors, changing the disease burden in yet unpredictable ways. Aedes aegypti is a mosquito responsible for transmitting dengue, Zika, chikungunya, and yellow fever viruses that breeds in containers associated with urban environments. We sought to understand how ambient temperature and larval densities in the immature aquatic phases determine adult life history traits and dengue virus loads post-infection. We predicted that larval crowding and high temperatures would both lead to smaller mosquitoes that might struggle to invest in an immune response and, hence, would exhibit high viral loads.

Methods We first examined larval densities from urban and rural areas via a meta-analysis. We then used these data to inform a laboratory-based 2×2 design examining the interacting effects of temperature (21 vs. 26°C) and density (0.2 vs. 0.4 larvae/mL) on adult life history and dengue virus loads.

Results We found that urban areas had an ~8-fold increase in larval densities compared to more rural sites. In the lab, we found that crowding had more impact on mosquito traits than temperature. Crowding led to slower development, smaller mosquitoes, less survival, lower fecundity, and higher viral loads, as predicted. The higher temperature led to faster development, reduced fecundity, and lower viral loads. The virus-reducing effect of higher temperature rearing was, however, overwhelmed by the impact of larval crowding when both factors were present.

Conclusions These data reveal complex interactions between the environmental effects experienced by immature mosquitoes and adult traits. They especially highlight the importance of crowding with respect to adult viral loads. Together, these data suggest that urban environments might enhance dengue virus loads and, therefore, possibly transmission, a concerning result given the increasing rates of urbanization globally.

Dutra HLC, Marshall DJ, Comerford B, McNulty BP, Diaz AM, Jones MJ, Mejia AJ, Bjornstad ON, McGraw EA (2024) Larval crowding enhances dengue virus loads in Aedes aegypti, a relationship that might increase transmission in urban environments, PLOS Neglected Tropical Diseases. 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