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

Authors: Dustin J Marshall, Hayley E Cameron, and Michel Loreau

Published in: The ISME (International Society for Microbial Ecology) Journal

Introduction

In their simplest form, the dynamics of populations are described in terms of two parameters: r, the intrinsic rate of increase; and K, the carrying capacity of the population. These two parameters are fundamental to population ecology and have a long history of empirical and theoretical study. From an evolutionary perspective, r and K were used to define and describe different modes of life: r-strategists were thought to have fast population growth rates at the expense of poor competitive abilities; K-strategists were thought to have slow-growing populations but be superior competitors, or at least more efficient with regards to resources.

These concepts have strongly influenced microbial ecologists and evolutionary biologists — r and K are often expected to trade off against each other across genotypes, strains or species. Since then, the classification of r– and K-strategists has been adapted by microbiologists to describe copiotrophic and oligotrophic species of microorganisms, respectively.

The idea that it is difficult to have both fast growth and be efficient in the use of resources has intuitive appeal: multiple mechanistic models attempt to explain how and why we might observe trade-offs between r and K. However, empirical studies struggle to detect trade-offs between r and K at multiple levels of biological organisation and instead sometimes even detect ‘trade-ups’ where r and K positively covary. Even within the same microbial strains, different r-K relationships can be observed depending on environmental quality. Similarly, comparisons across species fail to reveal simple oligotrophy and copiotrophy (or r-K strategist) dichotomies — instead species often fall on a continuum between these two extremes. In fact, expectations about how r and K covary with each other are based on an unfortunate quirk of scientific fate…

Marshall DJ, Cameron HE, Loreau M (2023) Relationships between intrinsic population growth rate, carrying capacity and metabolism in microbial populations. The ISME Journal PDF DOI

Authors: Craig R White and Dustin J Marshall

Published in: Physiology

Abstract

Most explanations for the relationship between body size and metabolism invoke physical constraints; such explanations are evolutionarily inert, limiting their predictive capacity. Contemporary approaches to metabolic rate and life history lack the pluralism of foundational work.

Here, we call for reforging of the lost links between optimization approaches and physiology.

White CR, Marshall DJ (2023) How and why does metabolism scale with body mass? Physiology PDF DOI

Authors: George C Jarvis and Dustin J Marshall

Published in: The American Naturalist

Abstract

The evolution of internal fertilization has occurred repeatedly and independently across the tree of life. As it has evolved, internal fertilization has reshaped sexual selection and the covariances among sexual traits, such as testes size, and gamete traits. But it is unclear whether fertilization mode also shows evolutionary associations with traits other than primary sex traits. Theory predicts that fertilization mode and body size should covary, but formal tests with phylogenetic control are lacking.

We used a phylogenetically controlled approach to test the covariance between fertilization mode and adult body size (while accounting for latitude, offspring size, and offspring developmental mode) among 1,232 species of marine invertebrates from three phyla.

Within all phyla, external fertilizers are consistently larger than internal fertilizers: the consequences of fertilization mode extend to traits that are only indirectly related to reproduction.

We suspect that other traits may also coevolve with fertilization mode in ways that remain unexplored.

Jarvis GC, Marshall DJ (2023) Fertilization mode covaries with body size. The American Naturalist PDF DOI

Authors: Alexander Blake and Dustin J Marshall

Published in: Evolutionary Applications

Abstract

Copepods play a critical role in the carbon cycle of the planet – they mediate the sequestration of carbon into the deep ocean and are the trophic link between phytoplankton and marine food webs.

Global change stressors that decrease copepod productivity create the potential for catastrophic positive feedback loops. Accordingly, a growing list of studies examine the evolutionary capacity of copepods to adapt to the two primary stressors associated with global change: warmer temperatures and lower pH. But the evolutionary capacity of copepods to adapt to changing food regimes, the third major stressor associated with global change, remains unknown.

We used experimental evolution to explore how a 10-fold difference in food availability affects life history evolution in the copepod, Tisbe sp. over 2 years, and spanning 30+ generations.

Different food regimes evoked evolutionary responses across the entire copepod life history: we observed evolution in body size, size-fecundity relationships and offspring investment strategies.

Our results suggest that changes to food regimes reshape life histories and that cryptic evolution in traits such as body size is likely. We demonstrate that evolution in response to changes in ocean productivity will alter consumer life histories and may distort trophic links in marine foodchains. Evolution in response to changing phytoplankton productivity may alter the efficacy of the global carbon pump in ways that have not been anticipated until now.

Blake A, Marshall DJ (2023) Copepod life history evolution under high‐ and low‐food regimes. Evolutionary Applications PDF DOI

Authors: Giulia Ghedini and Dustin J Marshall

Published in: Current Biology

Summary

Competition drives rapid evolution, which, in turn, alters the trajectory of ecological communities. These eco-evolutionary dynamics are increasingly well-appreciated, but we lack a mechanistic framework for identifying the types of traits that will evolve and their trajectories. Metabolic theory offers explicit predictions for how competition should shape the (co)evolution of metabolism and size, but these are untested, particularly in eukaryotes.

We use experimental evolution of a eukaryotic microalga to examine how metabolism, size, and demography coevolve under inter- and intraspecific competition.

We find that the focal species evolves in accordance with the predictions of metabolic theory, reducing metabolic costs and maximizing population carrying capacity via changes in cell size. The smaller-evolved cells initially had lower population growth rates, as expected from their hyper-allometric metabolic scaling, but longer-term evolution yielded important departures from theory: we observed improvements in both population growth rate and carrying capacity. The evasion of this trade-off arose due to the rapid evolution of metabolic plasticity. Lineages exposed to competition evolved more labile metabolisms that tracked resource availability more effectively than lineages that were competition-free.

That metabolic evolution can occur is unsurprising, but our finding that metabolic plasticity also co-evolves rapidly is new. Metabolic theory provides a powerful theoretical basis for predicting the eco-evolutionary responses to changing resource regimes driven by global change. Metabolic theory needs also to be updated to incorporate the effects of metabolic plasticity on the link between metabolism and demography, as this likely plays an underappreciated role in mediating eco-evolutionary dynamics of competition.

Ghedini G, Marshall DJ (2023) Metabolic evolution in response to interspecific competition in a eukaryote. Current Biology PDF DOI

Authors: Craig R White and Dustin J Marshall

Published in: Journal of Experimental Biology

Abstract

Constraint-based explanations have dominated theories of size-related patterns in nature for centuries. Explanations for metabolic scaling — the way in which metabolism changes with body mass — have been based on the geometry of circulatory networks through which resources are distributed, the need to dissipate heat produced as a by-product of metabolic processes, and surface-area-to-volume constraints on the flux of nutrients or waste.

As an alternative to these constraint-based approaches, we recently developed a new theory that predicts that metabolic allometry arises as a consequence of the optimisation of growth and reproduction to maximise fitness within a finite life. Our theory is free of physical geometric constraints that limit the possibilities available to evolution, and we therefore argue that metabolic allometry can be explained without the need to invoke any of the assumed constraints traditionally imposed by metabolic theories. Our findings also suggest that metabolism, growth and reproduction have co-evolved to maximise fitness (i.e. lifetime reproduction) and that the observed patterns in these fundamental characteristics of life can similarly be explained by optimisation rather than constraint.

In this Centenary Commentary, we present an overview of our approach and a critique of its limitations. We propose a suite of empirical tests that we hope will move the field forward, discuss the dangers of model overparameterisation and highlight the need to remain open to non-adaptive hypotheses for the origin of biological patterns.

White CR, Marshall DJ (2023) Optimisation and constraint: explaining metabolic patterns in biology. Journal of Experimental Biology PDF DOI