Animals vary dramatically in size and biologists have long been fascinated with how other traits change along with size. Metabolism is one of those traits. Metabolic rates increase with size but not proportionally, and the struggle to describe and understand this non-proportional or allometric scaling relationship has a long history.

In their review of the subject, Craig White and Dustin Marshall initially return to the 1830s where physical properties that governed heat exchange were thought to dictate how metabolic rates scale with size. By the 1900s scientists had moved to disputing the exact nature of the ‘scaling’ relationship between size and metabolism.

After more than a century of study, the most reliable finding is that metabolism almost always scales hypo-allometrically with body mass, that is: metabolism increases with size but at a less than 1:1 ratio. A scaling exponent less than 1. So yes, elephants have faster metabolic rates than mice but not as much as you might expect — as body size increases, relative energy use decreases.

More recently, scientists have focused not only on how — but also why — does metabolism scale with body size? Debating this question has resulted in two polarised schools of thought.

The first, which includes Sarrus and Rameaux’s 1830s prediction around heat exchange, is that physical properties constrain the metabolic rate. So, the surface area of an organism can constrain metabolism through regulating heat dissipation, or the network of vessels delivering (usually) oxygen (e.g. blood vessels, trachea or gills), dictates the scaling of metabolic rate through physical constraints to the rate at which resources can be delivered.

The second school of thought takes an evolutionary approach where life history optimisation considers the combination of traits that maximises fitness. Craig and Dustin align with this philosophy. Their recent publication in Science proposed a life history optimisation model which predicts that animals most successful at reproducing are those that exhibit precisely the kind of disproportionate scaling of metabolism with size that we see in real life. And for Craig and Dustin, their work highlights a vital issue — the strong connection between metabolic traits and fitness components: changing one changes them all.

To demonstrate how polarised these two approaches have become, Craig and Dustin took a ‘research weaving’ approach. They found that papers based on the latest theories around the importance of physical constraints in metabolic scaling with body mass, (Dynamic Equilibrium Theory and Metabolic Theory of Ecology) did not cite or consider the other main theory base (Life History Optimisation and Pace of Life theory) and vice versa.

So where to next? Craig and Dustin think that constraint driven models would benefit from including optimisation and that examining how optimisation changes in the face of absolute constraints (e.g. organisms cannot be infinitely large or small or quick, and metabolic rates cannot be zero or infinitely high) would add some necessary limits to their own work.

Importantly they also provide some examples of how we can test these theories. They focus on the long-standing traditions of quantitative genetics to simplify conceptual arguments about how metabolic rate (co)varies with other traits and fitness and predict its evolution.

For Craig and Dustin, the crux of changing to a more pluralistic approach based on life history optimisation is that we may better understand how metabolic rate evolves in response to global change or anthropogenic pressures.

This research is published in the journal Physiology.

As this year’s winner of the Mike Cullen Research Fellow Award, Lesley Alton was awarded $5000 in research funds for her publication with Vanessa Kellerman that appeared in Nature Climate Change in 2023.

Professor Mike Cullen was Chair of Zoology at Monash from 1976 to 1992. He was a passionate advocate for early career researchers and also instrumental in bringing a more rigorous and quantitative approach to the behavioural sciences. The awards committee felt that Lesley and Vanessa’s publication was strongly aligned with Mike Cullen’s values.

But of course, science doesn’t just happen overnight and, in the Mike Cullen Lecture, Lesley detailed the trajectory of her research interests and how they led her to this point.

Lesley started her PhD at the University of Queensland in 2007 just after the first global assessment of amphibians had taken place. The assessment confirmed a global decline in amphibians including from seemingly pristine habitats. One of the competing hypotheses for amphibian declines was increased exposure to UV-B radiation associated with human-induced stratospheric ozone depletion. Lesley already knew that UV-B could have adverse effects on amphibian development when she started her PhD, but in nature, animals face many challenges, and so Lesley wanted to know if other sources of environmental stress interact with UV-B to have compounding negative effects on amphibians.

Lesley was not surprised to find that UV-B decreased survival in tadpoles but she was surprised to find that exposure to UV-B in combination with predatory cues decreased tadpole survival even further. She wondered if simultaneous exposure to these two stressors carried a greater metabolic cost than exposure to either of these stressors in isolation. By studying both the metabolic and behavioural responses of tadpoles to these stressors, Lesley found evidence that being exposed to UV-B is more energetically costly for tadpoles when they live with predators: tadpoles exposed to both stressors were less active, yet their metabolic rates remained elevated suggesting they were under more physiological stress than those exposed only to UV-B.

Lesley’s interests in the effects of UV-B continued when she took up her first postdoctoral position at Monash University, but this time she was interested in how it might affect mosquitoes. With UV-B predicted to increase in the tropics by the end of the century, Lesley wondered how this might affect the ability of mosquitoes to transmit pathogens like dengue virus, which is a growing threat to human populations living in tropical and subtropical regions. To study the effects of UV-B on mosquitoes, Lesley exposed developing mosquito larvae to very low doses of UV-B every day to determine if early-life exposure to UV-B could have long lasting effects on adult immune function and fitness. Worryingly, Lesley found that a UV-B dose that is 10­–30 lower than what is currently observed in the tropics made female mosquitoes much more likely to become infected with dengue virus, but it also reduced their survival and fecundity – an unexpected bonus for tropical regions?

In addition to her work on UV-B, Lesley also developed an interest in the effect of temperature on the metabolic rates of cold-blooded animals (ectotherms), which rely on the thermal conditions of their environment to regulate their body temperature. This interest began while working as a research assistant at the University of Queensland when she received a Journal of Experimental Biology Travelling Award to visit a lab group in the USA. This group were looking at the effects of temperature on the evolution of traits in fruit flies. So, another change of model species, but the trip allowed Lesley to use her expertise in measuring metabolic rates to test the century-old Metabolic Cold Adaptation Hypothesis. This hypothesis predicts that animals evolved at cold temperatures will have higher metabolic rates than those evolved at hot temperatures when measured together at the same temperature. This counter-intuitive effect of temperature on the evolution of metabolic rate is predicted to arise as a consequence of natural selection counteracting the slowing down of metabolic rate that occurs at colder temperatures by favouring those individuals with higher metabolic rates. However, because patterns consistent with the Metabolic Cold Adaptation Hypothesis are not always evident in nature, the hypothesis remains highly controversial.

By measuring the metabolic rates of flies that had evolved experimentally in the lab at different temperatures, Lesley conducted a robust test of the Metabolic Cold Adaptation Hypothesis, but did not find support for the hypothesis. Lesley is now investigating whether the Metabolic Cold Adaptation Hypothesis is borne out if flies evolve at different temperatures under conditions where food is more limited, a scenario that more accurately reflects nature.

We will have to wait and see whether temperature and nutrition interact to shape the evolution of metabolic rate in fruit flies. Lesley has also examined whether environmental factors influence the capacity of ectotherms to respond to climate warming through acclimation which, unlike evolution, occurs within an animal’s lifetime. While ectotherms are expected to have higher energy demands in a warmer world, many ectotherms can acclimate to higher temperatures by reducing the thermal sensitivity of their metabolic rates to offset these energy requirements to some extent. However, Lesley and Vanessa’s research in fruit flies has shown that nutritionally poor diets and species interactions can erode the energetic benefits of thermal acclimation.

A more in-depth summary of the award-winning publication on the effect of species interactions on the metabolic costs of climate warming demonstrates that to improve our understanding of the threat of climate warming to species we must study animal responses to temperature in combination with other environmental stressors.

This research is published in the journal Nature Climate Change.

For those that have been paying attention, you will be aware of our recent post on copepod evolution in high food and low food regimes. Despite the ongoing lockdowns, Alex Blake returned to the lab to follow individuals in a third generation of ‘common gardens’ throughout their whole life history. He measured growth, survival, probability of egg production, clutch size and egg size across the entire lifespan of individuals and used that data to compile population models.

Alongside his supervisor from Oxford University, Professor Tim Coulson, Alex wanted to know how food supply would affect population measures such as population growth rates, population size, age structure and size structure within populations. Alex and Tim compiled population models called Integral Projection Models; a mathematical modelling technique that essentially combines regression models of how traits change across the lifespan of individuals.

As with Alex’s previous work they did find differences between the food regimes. Copepods cultured in high food environments grew slightly faster to a smaller adult size, reached peak egg production younger and produced smaller eggs compared to copepods from low food environments. The high food copepods were also longer lived and had shorter generation times.

But Alex and Tim found these discrepancies didn’t translate to differences at the population level. Population growth rates, and age and size distributions within populations are projected to be similar at the different food supply regimes.

This is potentially good news for marine food webs; ocean productivity is expected to decline with climate change but Alex And Tim’s work suggests that even under lower food supply copepods will be able to evolve to deal with these harsher environments. But there could be costs. Changes in body size and reproductive outputs may have knock on effects for copepod consumers. Fish fry in particular, have been shown to be meticulous about the size of copepods they eat.

Alex and Tim emphasise that there is more work to be done. They were unable to untangle the effects of food supply from the effects of density; crowded environments could impact copepod life histories in a number of ways separate to the effects of food. They also suggest future work looks at whether life history evolution to food regimes is actually adaptive and not simply a result of non-adaptive forces such as drift. Reciprocal transplant experiments are the gold standard test for this question and Alex and Tim are keen to see them implemented.

This research is published in the journal Oikos.

Many of us are familiar with the idea that a bit of healthy competition can improve performance but can it affect metabolic rates, size and growth rates? Giulia Ghedini and Dustin Marshall asked this question for a single-celled alga and found that competition selects for smaller and more energy efficient cells.

Giulia and Dustin wanted to know whether predictions from the Metabolic theory of Ecology would hold true. Metabolic theory looks at the relationship between size and metabolic rate (rate of energy use) of individuals and makes predictions about population growth rates, maximum population size and maximum population biomass.

To test theoretical predictions Giulia and Dustin evolved populations of the green alga Dunaliella tertiolecta for 70 generations in three environments. They grew Dunaliella either on its own (no competition), with more Dunaliella(intraspecific competition) or with three other species of algae (interspecific competition). The focal populations of Dunaliella were inside dialysis bags so that they were physically isolated but still experienced changes to nutrient and light availability brought about by competition with other algae present outside the bags.

At 35 and 70 generations subsamples of the focal populations were moved into the same environment for several generations – a ‘common garden’. This allows researchers to distinguish between short term or ‘plastic’ responses to an environment from persistent ‘evolved’ changes.

Giulia and Dustin found that after 35 generations of evolution, cells that had evolved in the presence of competitors were smaller, reached greater population densities but got there more slowly (population growth rates were slower) than cells evolved without competitors. But after 70 generations, cells evolved in competitive environments had the same rates of population growth as cells evolved on their own and yet still managed to reach the same high maximum population densities.

The evolution of greater metabolic flexibility appeared to be the key to enable cells grown in a competitive environment to reach these high population growth rates and densities. By measuring photosynthesis and respiration at two time points, (when cells were low in number versus when cell numbers were very high), Giulia and Dustin could see that when resources are abundant, competition-evolved cells increase metabolic rates more than cells evolved without competition. And the reverse was true; when resources are scarce, competition-evolved cells are able to downregulate energy-capture and use, better than cells evolved without competition.

The evolution of enhanced metabolic flexibility was not anticipated by any theory and Giulia and Dustin are keen to see further studies testing if competition drives metabolic plasticity in other systems.

But the Metabolic Theory of Ecology did predict most of the other changes that the pair saw and so they likely represent a common response to competition. In other words, theory predicts the evolution of more energy efficient cells and it is the original relationship between size and metabolic rate that dictates whether those cells will be bigger or smaller. See also: Travelling in time: an experimental evolution experiment changes what we thought we know about size and the cost of reproduction.

This research is published in Current Biology.

As ocean temperatures soar to a one in a million-year event, many are wondering what this will mean for systems that receive less public attention than our iconic coral reefs. The oceans are a huge carbon sink and small planktonic crustaceans called copepods are a vital link in the planet’s carbon cycle.

Copepods eat phytoplankton, and phytoplankton productivity is likely to be affected by global warming in a number of ways. In some areas the boundary layer between the warmer surface waters and cooler, nutrient rich waters will reduce the delivery of nutrients to the surface waters. In other areas large storms will likely increase the nutrients delivered to surface. The result? Vastly different amounts of food available for the copepods that feed on phytoplankton

PhD student, Alex Blake, and supervisor Dustin Marshall compared the evolution of copepods under high and low food regimes. They were interested in life history traits – characteristics that describe the way an organism uses resources to increase the chance of successful reproduction. These types of measures have immediate knock-on effects for population growth rates.

In 2018 Alex randomly assigned copepods to high-food or low-food regimes with high-food cultures receiving 10 times the food supply of low food cultures. After approximately 30 generations of evolution Alex moved the copepods into a common environment where they received intermediate levels of food and he began measuring size, age at reproduction and reproductive output over successive generations.

Unfortunately for Alex this intense period of lab work coincided with one of Melbourne’s lengthy lockdowns. In order to comply with health and safety regulations during the long hours in the lab, fellow PhD students had to take turns keeping Alex company remotely. Alex was always visible to another lab member via Zoom while he worked his way through the copepod measurements.

When Alex and Dustin were able to get together and analyse the data they found that the different food regimes had evoked evolutionary changes in body size, the relationship between size and reproductive output and offspring investment strategies.

But the changes weren’t all straight forward. When Alex measured body size in the initial cultures as they entered the common environment, low-food copepods were slightly smaller than high-food copepods. After two generations in a common environment, low-food copepods were now bigger than high-food copepods. This counter-intuitive change is sometimes called cryptic evolution; copepods were smaller in response to the low-food environment, but this masked a genetic change where copepods had evolved the capacity to be bigger when the environment allowed.

At the same time Alex and Dustin found that larger mothers in the low-food cultures produced larger but slightly fewer offspring while high-food copepods produced smaller but more offspring. When combined, these two components of reproduction result in the low-food copepods having a steeper positive relationship between maternal size and reproductive output. So, for two large mothers, the low-food mother will have a greater reproductive output than the high-food mother.

Alex and Dustin speculated that the evolution of low-food copepods to be bigger was driven by selection on larger mothers having a greater reproductive output. While they can’t say for sure why low-food copepods had evolved the capacity to be bigger when the environment allowed, they do emphasise that this example of cryptic evolution means that 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.

This research was published in Evolutionary Applications.