Annual Report 2018

 

The Centre for Geometric Biology is developing and testing a new theory for how and why organisms grow.

Our particular focus is on how the net flux of energy (the energy acquired through food, photosynthesis, or chemosynthesis minus the energy lost to metabolism) changes with size, whether it be cell size or total body size.

Centre overview

The Centre for Geometric Biology (CGB) was established in 2015 within the School of Biological Sciences at Monash University and had the following primary objective:

  • To establish Monash University as the founder of the field of Geometric Biology, changing the way we study, understand and manage natural systems.

In order to achieve this aim, the CGB planned to focus on the following activities:

  • Promote an interdisciplinary approach across the biological sciences
  • Strengthen international ties
  • Communicate the Geometric Theory of Biology
  • Demonstrate the applied value of the theory.

Director’s message

As we near the end of the 4th year of the Centre for Geometric Biology, we are able to take stock and reflect on our progress towards our objectives.  The Centre continues to grow with increased involvement from a range of research staff within the School for Biological Sciences here at Monash University and collaborations with colleagues from other universities.

2018 has been a pivotal year for the Centre for Geometric Biology, in that some of the original thinking and discussions between Craig and myself that led to the inception of the Centre, have crystallized and made it into journals.  We received an invitation to publish a review in the journal ‘Trends in Evolutionary Ecology’.  This review was a culmination of many discussions and reflects some of our core thinking around the theory of geometric biology.  In addition we were also able to demonstrate the applied value of the theory with a paper in Science that applies the theory of geometric biology to fisheries management and details the very real problems associated with incorrect assumptions about investment into reproduction.

We have been working hard to address some of the recommendations from the internal review of the Centre that took place in 2017 and, in particular, have focused on the theoretical base of our work.  Collaborations with mathematical modeller, Professor Tim Coulson (Oxford University) and theoretician, Professor Troy Day, (Queens University, Ontario), continue and have been strengthened by the appointment of a postdoctoral researcher (Melissa Verin) to work with ourselves and Troy in Canada.

We have also been striving to create a more cohesive community and to this end have been running bi-monthly meetings of research updates or information sessions for graduate students and Early Career Researchers.  We have been delighted to see the involvement of Centre members of all career levels at these meetings.

We are also pleased to announce the continued support from the Provost and the School of Biological Sciences who have provided funding for further data mining.  2019 will see us intensifying our efforts in that area.

Director, Dustin Marshall and Deputy Director, Craig White.


Looking back: research highlights 2018

While choosing research highlights is never easy, we present four studies, chosen to emphasise our progress in the core thinking of the Centre, the range of approaches and organisms we work with as well as the applications of a geometric biology approach.

Growing Pains: time to reassess models of growth?

A central aim of the Centre for Geometric Biology is understanding how and why organisms grow. In a recent opinion piece, published in the journal Trends in Ecology & Evolution, Dustin Marshall and Craig White suggest that it might be time to take another look at the ways we currently understand and model growth.

In the past, growth has mainly been considered in two different ways. Mechanistic models of growth emphasise identifying the physiological processes driving growth. This group of models includes the von Bertalanffy Growth Function, which is perhaps the best-known growth model. It estimates the rate of increase in mass (growth) as the difference between anabolism (energy-consuming processes) and catabolism (energy-producing processes). Other models of this type include the Ontogenetic Growth Model and the Dynamic Energy Budget model.

In contrast, phenomenological models of growth are based on life-history theory and work from the assumption that organisms evolve to maximise their fitness. Theories and models under this framework revolve around the trade-offs between maximising reproduction against the risk of mortality.

The von Bertalanffy Growth Function and more recent mechanistic models do an excellent job of describing how the growth of most organisms slows as they approach their final size. Models such as these assume that growth slows or stops because the organism cannot acquire, distribute or use resources faster than it has to expend them on self-maintenance.

There is a problem however. Mechanistic models do not adequately consider reproduction — an energetically expensive undertaking. Most mechanistic models make the simple but crucial assumption that reproduction is proportional to body size, and that allocation to reproduction begins at birth and remains a constant fraction of total body size throughout an individual’s life. While this assumption seems unrealistic, it is essential for these models to describe growth well.

Phenomenological models tend to have different dynamics for juvenile and mature phases; after maturity, increasing allocation of resources to reproduction reduces growth. But again, most of these models assume that reproductive output is directly proportional to body size.

We now know that, for marine fish at least, reproductive output is disproportionally higher in bigger females. Dustin and Craig suspect that this pattern is the rule for most taxa but that it has been overlooked (see Figure 1).  If this does occur more generally, what does it mean for our understanding of growth?

Figure 1. Data from a range of taxa (A = marine invertebrates and B = other taxa) showing the disproportionate increase in reproductive output at larger sizes. The dotted line in each case shows what a 1:1 (or isometric) scaling of reproduction with growth would look like.

Dustin and Craig argue that many of the mechanistic models of growth are trying to explain dynamics that are driven by increasing allocation to reproduction but they do not allow for it.  Instead, these models assume that resource supply decreases as individuals get bigger so that if the allocation to reproduction is allowed to increase then organisms will shrink once they start to reproduce.

A common feature of both theoretical approaches is that they assume that the relative amount of energy available for total production decreases with size.  If we instead assume that resource acquisition and usage both change in the same proportions in relation to size, and combine those parameters with the disproportionate increase in reproductive output (hyperallometry), then we can predict growth trajectories remarkably well (see Figure 2).

Dustin and Craig posit that the growth dynamics that biologists have long sought to understand emerge simply from hyperallometric scaling of reproduction.

Figure 2. Dustin and Craig propose a simple model that allows energy intake and expenditure to scale consistently with size, but reproductive output to increase disproportionately with size. To illustrate that this “hyperallometric reproduction” model describes growth patterns on par with well-known mechanistic models, Dustin and Craig have used data for cod Gadus morhua and have fitted model outputs for the van Bertanalaffy Growth Function (orange), the Ontogentic Growth Model (blue) and the hyperallometric reproduction model shown in red.

Bigger is better when it comes to female fish and feeding the planet

An international study led by the Centre for Geometric Biology has found that larger fish are much more important to feeding the planet than previously thought.

The research confirmed what field biologists have long suggested: that larger mothers reproduced disproportionately much more than smaller ones. Furthermore, larger mothers may produce offspring that perform better and are more likely to survive to adulthood.

The findings clash with current theories. And the results have major implications for fisheries, the value placed on marine protected areas, the impacts of climate change and the 20% of people globally who rely on fish for protein.

The Centre’s Diego Barneche, Craig White, and Dustin Marshall, with Ross Robertson from The Smithsonian Tropical Research Institute, collated and analysed data from 342 species of fish across 14 orders gathered from studies undertaken over a 100-year time span. The team were particularly interested in understanding the relationships between female size and the number of eggs produced, egg volume and egg energy content.

Most life-history theories assume that reproductive output increases proportionately with female size; for every unit increase in female size, there is a proportional increase in reproductive output.  That is, the combined reproductive output of two one-kilogram fish is assumed to be the same as a single two-kilogram fish. But for the overwhelming majority of species, the research team found that overall reproductive output increased disproportionately with female body size. Bigger is much, much better.

The consequences for fisheries cannot be understated. Reproductive output drives population replenishment, and larger fish are much more important for the replenishment of marine fish populations than previously assumed. Outdated models for sustainable harvesting of fish populations are fundamentally flawed.

Our models of how organisms grow and reproduce are based on the wrong assumptions, and as a consequence we are overharvesting wild populations with calamitous consequences.Dustin Marshall

The costs of global change make the study findings even more stark. Climate change is predicted to cause fish body sizes to decrease. Warmer oceans will likely have fewer (and smaller) fish, and drastically reproductive output.

But the research also points to some good news, suggesting that current conservation strategies are more potent than previously thought.  Marine protected areas have been shown to increase fish size by 28% on average. That means that the per-capita reproductive output of fish inside these areas will be much higher than is generally appreciated.

Our discovery means that the benefits of marine protected areas have been massively underestimated, they produce far more new fish than unprotected areas of the same size.Dustin Marshall

This research is published in the Journal Science.

How do mutations affect growth and fermentation rates in yeast?

In the yeast Saccharomyces cerevisiae, glucose is converted to energy in oxygenated environments via fermentation rather than respiration.  Scientists are curious to discover why there is this preference for a relatively inefficient method of utilising glucose.

Aysha Sezmis and colleagues from the McDonald and Marshall labs within the Centre for Geometric Biology are looking at this question through the lens of evolutionary biology.  They recognised that although fermentation might be less efficient than respiration, it converts glucose into energy more quickly than respiring competitors.  In populations that have evolved with abundant resources, individuals that most rapidly convert resource into biomass and energy are favoured, even at the cost of efficiency.

Aysha and her colleagues were interested to find out whether mutations that have appeared repeatedly in experimental populations of yeast allowed the mutant populations to achieve greater fitness through their ability to ferment glucose at a wider range of glucose concentrations.

They re-created 6 mutations that repeatedly evolve in yeast evolution experiments by using a gene deletion technique and grew the different yeast populations in varying concentrations of glucose and ammonium sulphate.  Across these concentration gradients, they were able to detect if fermentation was the preferential method for acquiring energy by measuring ethanol; a metabolite of fermentation.  They then compared these rates with those of the ancestral population.  They were able to measure growth rates, maximum yields and fitness for each population at each combination of glucose and nitrogen concentration.

A ‘heat map’ showing the amount of ethanol produced for each of the six strains of the yeast S. cerevisiae at different nitrogen and glucose concentrations.

The team found that simple selection for high growth rates can drive the evolution of a preference for fermentation at glucose concentrations where respiration is preferred by the ancestral strain.  But most interestingly they found that nitrogen concentrations also played a part and the fermentation phenotype may only be ‘engaged’ at very low nitrogen concentrations.  They concluded that the mounting evidence for the importance of nitrogen abundance in the switch from respiration to fermentation as a preferred mechanism should be considered in future studies.

 

Time to go back to school? Geometry helps predict change in ecosystem function

Humans are continually modifying the marine environment either directly, with activities such as fishing, or indirectly as with climate change or the introduction of invasive species. A common consequence of these activities is a change in the body size of individuals that make up an ecological community. 

Understanding the impacts of such changes on the way in which communities gain and use energy is of particular interest to Giulia Ghedini, a post-doc in the Centre for Geometric Biology.

“We know that human impacts can change the size of organisms and we also know that the size of an organism determines the speed at which it uses resources and contributes to the flow of energy within a system” explains Dr Ghedini.

“Understanding how changes in the ‘geometry’ of a whole community might affect ecosystem functioning through changes in metabolic rates is not only theoretically interesting but of practical significance as well” she said. 

Metabolism measurements indicate how much oxygen and food an individual, or an entire community, consumes. Understanding how changes in individual body size affect the energy use of whole communities provides direct information on the amount of resources required for these communities to live. 

Researchers from the Centre for Geometric Biology at Monash University were able to test predictions that older communities, made up of larger organisms, would have lower metabolic rates per unit mass than younger communities of smaller individuals. 

“We know that increases in metabolic rates slow down as organisms get larger – and we wanted to know if this same pattern occurs at the level of whole communities” said Dr Ghedini.

To their surprise, the research team found that the community metabolic rates remained directly proportional to total community mass as communities got older and larger, which contrasted with the way metabolic rate scaled with changes in size of the dominant species. 

“But,” said Dr Ghedini “when we deconstructed the community into individuals and calculated their individual metabolic rates based on their size and species-specific metabolism, we found that community rates were largely the sum of their parts with respect to metabolism.” 

Measuring metabolism of a whole community can be hard, and so studies frequently estimate community metabolism from the dominant species in that community; we now know that for these estimates to be accurate we need to know the sizes of the individuals that make up the community.

“We also found that as communities got older, the same area was able to support much higher biomasses and energy use – three times as much as the younger communities. We attributed this to changes in the shape of the community; that is, a more 3D structure allowed certain individuals greater access to food in the water column and increased oxygen delivery via increased water flow.”

Changes in rates of energy use have long been used as an indicator of change in ecosystem function. 

By unravelling the relationship between the size of individuals and the energy use of whole communities, this study will help us predict how changes in the geometry of communities will impact on the use of resources; a measure of ecosystem function.

This research was published in a special issue of the journal Functional Ecology.


Looking forward: some upcoming projects in 2019

A number of large new projects will be getting underway in 2019 as a result of ARC funding schemes. Dustin Marshall and Matt Hall are now Future Fellows and Giulia Ghedini has received a Discovery Early Career Researcher Award. Dustin and Giulia will be using marine invertebrates to look into impacts of global warming whilst Matt is tackling the importance of sex in the evolution of infectious disease.

At the same time a CGB funded collaboration with Dustin, Craig and Mike McDonald will be looking at how metabolic rate scales with temperature in 60,000 generations of E. coli.

Matt is considering the role sex plays in the evolution of infectious disease.

Within a given species, often the greatest heterogeneity that a pathogen will encounter will be due to differences between males and females. Yet, up until recently, insight into this crucial topic was driven by research into one sex, typically males.

Matt’s recent work has shown that, in the water-flea Daphnia magna, not only is pathogen fitness lower in males, but so is a pathogen’s evolutionary potential. What is more, the relative proportion of males in a population can fundamentally alter the overall transmission potential of a pathogen.

Matt has demonstrated that pathogen fitness is sex specific; in this case pathogen fitness is greater in females (left graph).  More recent work of Matt’s has found that changes in the relative proportion of males can increase the burden of disease for every individual (right graph).

This project was stimulated by Matt’s recognition that there is an absence of theory that explicitly considers how males and females can impact on the evolution and epidemiology of infectious disease.  Matt is seeking to address this imbalance and integrate sex-specific effects into a general framework for disease evolution and epidemiology.

Matt will be using the water-flea Daphnia magnaand its associated pathogens to provide an experimental system in which he can manipulate infections in males and females, characterise the degree of differentiation, and generate predictive models.

Dustin will be investigating how temperature affects the life-history stages of feeding and non-feeding larvae. Marine life histories show strong biogeographic patterns: warmer waters favour species with feeding larvae and cooler waters favour species with non-feeding larvae. Warming could be particularly problematic for Australian species because in 2012, Dustin discovered that Australian coastal species predominantly have non-feeding larvae. This means that future temperatures increases could affect native Australian invertebrates disproportionately relative to other regions of the world. (Put in schematic from application here)

Schematic of the data pipeline to estimate developmental energetics across temperature regimes. For each species, parents will be exposed to a range of temperatures, after which the size and number of offspring that are produced will be measured. These offspring will then have every phase of their energy usage and acquisition, from fertilisation through to metamorphosis estimated across an orthogonal temperature range. Dustin will then integrate these estimates to create a thermal energy performance curve for each species and use these data to parameterise models of connectivity, viability and life history evolution.

At the end of an intensive experimental period, Dustin will have quantitative estimates of how temperature alters the success of a range of species from the gamete to the juvenile. At this stage Dustin will work with collaborators to generate predictive models to determine

  1. how does temperature alter the relative advantages for each of the two developmental modes?
  2. how does temperature affect dispersal and connectivity among populations for each developmental mode? and finally
  3. how does temperature affect the distribution of marine organisms with feeding or non-feeding larvae?

Giulia will be investigating how global warming will affect entire ecological communities.

We already know that warming can affect individuals by reducing their body size and speeding up energy use, as well as reducing water viscosity.  But what we don’t know is how these changes at the individual level might play out at the population and community level and affect the energy intake or expenditure of whole communities.

Giulia will be looking at how changes in body size at the individual level interact with population and community level ecosystem functions.

Giulia is particularly interested in this knowledge gap and will be investigating the implications of warming sea temperatures for important ecosystem functions such as productivity, food web stability or resistance to invasion.

Giulia has planned a series of experiments, using communities of easily manipulated, sessile, marine invertebrates, to explore 4 main questions.

  1. How do changes in community size-structure and composition under warming alter the energy intake (phytoplankton) and expenditure (oxygen) of marine invertebrate communities?
  2. Since the availability of energy can mediate biological invasions, does warming alter the energy usage of communities so that they are more susceptible to invasive species?
  3. Are the responses of invertebrate communities to warming mediated by changes in their food (phytoplankton)?
  4. Given that warming reduces water viscosity, how does this mechanical effect alter food consumption and metabolic expenditure in marine communities of different size-structure?

CGB quick view

Publications
71
scientific publications since CGB began in 2015
27
publications from the CGB in 2018
79.4%
publications in top 10% journals by Cite Score
244
citations received by publications 2015-2018

(Stats from Scopus and SciVal 11 January 2019 based on 71 publications identified by Scopus)

Communications
46
posts published on website in 2018
4,742
website visitors in 2018
100
tweets in 2018
1
article in top 5% of all research outputs scored by Altmetric in 2018 (Source: Altmetric 11 January 2019)

 

Management structure
7
members of the advisory committee
2
members of the management committee
5
directly funded staff members
11
affiliated group leaders within School of Biological Sciences

 

Events
2
international visitors hosted
2
Australian visitors hosted
4
CGB discussion groups
3
student / early career researcher information sessions
1
leaders’ lunch

Staff news

There have been a few changes in the core staff who are directly funded by the CGB. We said goodbye to Diego Barneche in 2017 after he completed his 2 year post doc and after a year at UNSW Diego is moving to Exeter to start a lectureship position. Martino Malerba and Giulia Ghedini remain as post docs within the Centre but Giulia has secured her own funding in the form of an ARC DECRA to start in 2019, whilst Martino will be applying for a DECRA next year. Melissa Verrin is also an affiliated Centre post-doc based at Queens University in Canada to allow ongoing collaboration with theoretical biologist, Professor Troy Day.  We will also be welcoming another post doc to the Centre in early 2019 – Mariana Alvarez Noriega. Lucy Klein, the Centre RA has also moved on and we are pleased to welcome Tormey Reimer to the CGB.

The management committee, Dustin Marshall and Craig White, remain and are primary supervisors to nine PhD students. Amanda Pettersen, co-supervised by Dustin and Craig was awarded her PhD in 2018. Dustin coordinates the undergraduate course Marine Ecology and Craig teaches in the Humans, evolution and modern society course that was rolled out in 2017.


Full publications list

Arnold, P.A., Cassey, P. & White, C.R. (2017) Functional traits in red flour beetles: the dispersal phenotype is associated with leg length but not body size nor metabolic rate. Functional Ecology,31,653-661.

Arnold, P.A., Rafter, M.A., Malekpour, R., Cassey, P., Walter, G.H. & White, C.R. (2017) Investigating movement in the laboratory: dispersal apparatus designs and the red flour beetle, Tribolium castaneum. Entomologia Experimentalis et Applicata,163,93-100.

Barneche, D.R. & Allen, A.P. (2018) The energetics of fish growth and how it constrains food-web trophic structure.Ecology Letters,21,836-844.

Barneche, D.R., Burgess, S.C. & Marshall, D.J. (2018) Global environmental drivers of marine fish egg size. Global Ecology and Biogeography,27,890-898.

Barneche, D.R., Ross Robertson, D., White, C.R. & Marshall, D.J. (2018) Fish reproductive-energy output increases disproportionately with body size. Science,360,642-645.

Barneche, D.R., White, C.R. & Marshall, D.J. (2017) Temperature effects on mass-scaling exponents in colonial animals: A manipulative test. Ecology,98,103-111.

Bay, S., Ferrari, B. & Greening, C. (2018) Life without water: How do bacteria generate biomass in desert ecosystems? Microbiology Australia,39,28-32.

Bender, M.G., Leprieur, F., Mouillot, D., Kulbicki, M., Parravicini, V., Pie, M.R., Barneche, D.R., Oliveira-Santos, L.G.R. & Floeter, S.R. (2017) Isolation drives taxonomic and functional nestedness in tropical reef fish faunas. Ecography,40,425-435.

Bywater, C.L., Wilson, R.S., Monro, K. & White, C.R. (2018) Legs of male fiddler crabs evolved to compensate for claw exaggeration and enhance claw functionality during waving displays. Evolution,72,2491-2502.

Cameron, H., Monro, K., Malerba, M., Munch, S. & Marshall, D. (2016) Why do larger mothers produce larger offspring? A test of classic theory. Ecology,97,3452-3459.

Cameron, H., Monro, K. & Marshall, D.J. (2017) Should mothers provision their offspring equally? A manipulative field test. Ecology Letters,20,1025-1033.

Cantor, M., Pires, M.M., Marquitti, F.M.D., Raimundo, R.L.G., Sebastián-González, E., Coltri, P.P., Perez, S.I., Barneche, D.R., Brandt, D.Y.C., Nunes, K., Daura-Jorge, F.G., Floeter, S.R. & Guimarães, P.R. (2017) Nestedness across biological scales. PLoS ONE,12.

Carere, C.R., Hards, K., Houghton, K.M., Power, J.F., McDonald, B., Collet, C., Gapes, D.J., Sparling, R., Boyd, E.S., Cook, G.M., Greening, C. & Stott, M.B. (2017) Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME Journal,11,2599-2610.

Chang, C.Y. & Marshall, D.J. (2016) Spatial pattern of distribution of marine invertebrates within a subtidal community: do communities vary more among patches or plots? Ecology and Evolution,6,8330-8337.

Chang, C.Y. & Marshall, D.J. (2017) Quantifying the role of colonization history and biotic interactions in shaping communities –a community transplant approach. Oikos,126.

Chirgwin, E., Marshall, D.J., Sgrò, C.M. & Monro, K. (2017) The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change? Evolutionary Applications,10,267-275.

Chirgwin, E., Marshall, D.J., Sgrò, C.M. & Monro, K. (2018) How does parental environment influence the potential for adaptation to global change? Proceedings of the Royal Society B: Biological Sciences,285.

Connallon, T. & Hall, M.D. (2018) Genetic constraints on adaptation: a theoretical primer for the genomics era. Annals of the New York Academy of Sciences,1422,65-87.

Connallon, T., Sharma, S. & Olito, C. (2019) Evolutionary consequences of sex-specific selection in variable environments: Four simple models reveal diverse evolutionary outcomes. American Naturalist,193,93-105.

Crean, A.J. & Marshall, D.J. (2015) Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae). Marine Biology,162,2251-2256.

Dong, X., Greening, C., Brüls, T., Conrad, R., Guo, K., Blaskowski, S., Kaschani, F., Kaiser, M., Laban, N.A. & Meckenstock, R.U. (2018) Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats. ISME Journal,12,2039-2050.

Dubuc, A., Waltham, N., Malerba, M. & Sheaves, M. (2017) Extreme dissolved oxygen variability in urbanised tropical wetlands: The need for detailed monitoring to protect nursery ground values. Estuarine, Coastal and Shelf Science,198,163-171.

Dunn, R.E., White, C.R. & Green, J.A. (2018) A model to estimate seabird field metabolic rates. Biology Letters,14.

Ghedini, G. & Connell, S.D. (2017) Moving ocean acidification research beyond a simple science: Investigating ecological change and their stabilizers. Food Webs,13,53-59.

Ghedini, G., Loreau, M., White, C.R. & Marshall, D.J. (2018) Testing MacArthur’s minimisation principle: do communities minimise energy wastage during succession? Ecology Letters,21,1182-1190.

Ghedini, G., White, C.R. & Marshall, D.J. (2017) Does energy flux predict density-dependence? An empirical field test. Ecology,98,3116-3126.

Ghedini, G., White, C.R. & Marshall, D.J. (2018) Metabolic scaling across succession: Do individual rates predict community-level energy use? Functional Ecology,32,1447-1456.

Gipson, S.A.Y. & Hall, M.D. (2018) Interactions between host sex and age of exposure modify the virulence–transmission trade-off. Journal of Evolutionary Biology,31,428-437.

Good, B.H., McDonald, M.J., Barrick, J.E., Lenski, R.E. & Desai, M.M. (2017) The dynamics of molecular evolution over 60,000 generations. Nature,551,45-50.

Grémillet, D., White, C.R., Authier, M., Dorémus, G., Ridoux, V. & Pettex, E. (2017) Ocean sunfish as indicators for the ‘rise of slime’. Current Biology,27,R1263-R1264.

Hachich, N.F., Bonsall, M.B., Arraut, E.M., Barneche, D.R., Lewinsohn, T.M. & Floeter, S.R. (2016) Marine island biogeography. Response to comment on ‘Island biogeography: patterns of marine shallow-water organisms’. Journal of Biogeography,43,2517-2519.

Halsey, L.G. & White, C.R. (2017) A different angle: Comparative analyses of whole-animal transport costs when running uphill. Journal of Experimental Biology,220,161-166.

Ji, M., Greening, C., Vanwonterghem, I., Carere, C.R., Bay, S.K., Steen, J.A., Montgomery, K., Lines, T., Beardall, J., Van Dorst, J., Snape, I., Stott, M.B., Hugenholtz, P. & Ferrari, B.C. (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature,552,400-403.

Lagos, M.E., Barneche, D.R., White, C.R. & Marshall, D.J. (2017) Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions. Global Change Biology,23,2321-2330.

Lagos, M.E., White, C.R. & Marshall, D.J. (2016) Biofilm history and oxygen availability interact to affect habitat selection in a marine invertebrate. Biofouling,32,645-655.

Lagos, M.E., White, C.R. & Marshall, D.J. (2017) Do invasive species live faster? Mass-specific metabolic rate depends on growth form and invasion status. Functional Ecology,31,2080-2086.

Lange, R. & Marshall, D. (2017) Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Scientific Reports,7.

Lange, R., Monro, K. & Marshall, D.J. (2016) Environment-dependent variation in selection on life history across small spatial scales. Evolution,70,2404-2410.

Lawton, R.J., Paul, N.A., Marshall, D.J. & Monro, K. (2017) Limited evolutionary responses to harvesting regime in the intensive production of algae. Journal of Applied Phycology,29,1449-1459.

Liedke, A.M.R., Barneche, D.R., Ferreira, C.E.L., Segal, B., Nunes, L.T., Burigo, A.P., Carvalho, J.A., Buck, S., Bonaldo, R.M. & Floeter, S.R. (2016) Abundance, diet, foraging and nutritional condition of the banded butterflyfish (Chaetodon striatus) along the western Atlantic. Marine Biology,163,1-13.

Malerba, M.E., Palacios, M.M. & Marshall, D.J. (2018) Do larger individuals cope with resource fluctuations better? An artificial selection approach. Proceedings of the Royal Society B: Biological Sciences,285.

Malerba, M.E., Palacios, M.M., Palacios Delgado, Y.M., Beardall, J. & Marshall, D.J. (2018) Cell size, photosynthesis and the package effect: an artificial selection approach. New Phytologist,219,449-461.

Malerba, M.E., White, C.R. & Marshall, D.J. (2017) Phytoplankton size-scaling of net-energy flux across light and biomass gradients. Ecology,98,3106-3115.

Malerba, M.E., White, C.R. & Marshall, D.J. (2018) Eco-energetic consequences of evolutionary shifts in body size. Ecology Letters,21,54-62.

Marshall, D.J., Burgess, S.C. & Connallon, T. (2016) Global change, life-history complexity and the potential for evolutionary rescue. Evolutionary Applications,9,1189-1201.

Marshall, D.J., Lawton, R.J., Monro, K. & Paul, N.A. (2018) Biochemical evolution in response to intensive harvesting in algae: Evolution of quality and quantity. Evolutionary Applications,11,1389-1400.

Marshall, D.J., Pettersen, A.K. & Cameron, H. (2018) A global synthesis of offspring size variation, its eco-evolutionary causes and consequences. Functional Ecology,32,1436-1446.

Marshall, D.J. & White, C.R. (2018) Have We Outgrown the Existing Models of Growth? Trends in Ecology and Evolution.

Monro, K. & Marshall, D.J. (2016) Unravelling anisogamy: Egg size and ejaculate size mediate selection on morphology in free-swimming sperm. Proceedings of the Royal Society B: Biological Sciences,283.

Nang, S.C., Morris, F.C., McDonald, M.J., Han, M.L., Wang, J., Strugnell, R.A., Velkov, T. & Li, J. (2018) Fitness cost of mcr-1-mediated polymyxin resistance in Klebsiella pneumoniae. Journal of Antimicrobial Chemotherapy,73,1604-1610.

Naya, D.E., Naya, H. & White, C.R. (2018) On the interplay among ambient temperature, basal metabolic rate, and body mass. American Naturalist,192,518-524.

Ohmer, M.E.B., Cramp, R.L., Russo, C.J.M., White, C.R. & Franklin, C.E. (2017) Skin sloughing in susceptible and resistant amphibians regulates infection with a fungal pathogen. Scientific Reports,7.

Olito, C. (2017) Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites. Evolution,71,458-464.

Olito, C. & Marshall, D.J. (2018) Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae). Journal of Evolutionary Biology.

Olito, C., White, C.R., Marshall, D.J. & Barneche, D.R. (2017) Estimating monotonic rates from biological data using local linear regression. Journal of Experimental Biology,220,759-764.

Pettersen, A.K., Marshall, D.J. & White, C.R. (2018) Understanding variation in metabolic rate. Journal of Experimental Biology,221.

Pettersen, A.K., White, C.R., Bryson-Richardson, R.J. & Marshall, D.J. (2018) Does the cost of development scale allometrically with offspring size? Functional Ecology,32,762-772.

Pettersen, A.K., White, C.R., Bryson-Richardson, R.J. & Marshall, D.J. (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters.

Pettersen, A.K., White, C.R. & Marshall, D.J. (2016) Metabolic rate covaries with fitness and the pace of the life history in the field. Proceedings of the Royal Society B: Biological Sciences,283.

Polymeropoulos, E.T., Oelkrug, R., White, C.R. & Jastroch, M. (2017) Phylogenetic analysis of the allometry of metabolic rate and mitochondrial basal proton leak. Journal of Thermal Biology,68,83-88.

Portugal, S.J., Ricketts, R.L., Chappell, J., White, C.R., Shepard, E.L. & Biro, D. (2017) Boldness traits, not dominance, predict exploratory flight range and homing behaviour in homing pigeons. Philosophical Transactions of the Royal Society B: Biological Sciences,372.

Portugal, S.J., Sivess, L., Martin, G.R., Butler, P.J. & White, C.R. (2017) Perch height predicts dominance rank in birds. Ibis,159,456-462.

Prokopuk, L., Stringer, J.M., White, C.R., Vossen, R.H.A.M., White, S.J., Cohen, A.S.A., Gibson, W.T. & Western, P.S. (2018) Loss of maternal EED results in postnatal overgrowth. Clinical Epigenetics,10.

Sezmis, A.L., Malerba, M.E., Marshall, D.J. & McDonald, M.J. (2018) Beneficial Mutations from Evolution Experiments Increase Rates of Growth and Fermentation. Journal of Molecular Evolution,86,111-117.

Svanfeldt, K., Monro, K. & Marshall, D.J. (2017) Dispersal duration mediates selection on offspring size. Oikos,126,480-487.

Svanfeldt, K., Monro, K. & Marshall, D.J. (2017) Field manipulations of resources mediate the transition from intraspecific competition to facilitation. Journal of Animal Ecology,86,654-661.

Svanfeldt, K., Monro, K. & Marshall, D.J. (2018) Resources mediate selection on module longevity in the field. Journal of Evolutionary Biology,31,1666-1674.

Tate, M., McGoran, R.E., White, C.R. & Portugal, S.J. (2017) Life in a bubble: the role of the labyrinth organ in determining territory, mating and aggressive behaviours in anabantoids. Journal of Fish Biology,91,723-749.

Uesugi, A., Connallon, T., Kessler, A. & Monro, K. (2017) Relaxation of herbivore-mediated selection drives the evolution of genetic covariances between plant competitive and defense traits. Evolution,71,1700-1709.

Wannier, T.M., Kunjapur, A.M., Rice, D.P., McDonald, M.J., Desai, M.M. & Church, G.M. (2018) Adaptive evolution of genomically recoded Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America,115,3090-3095.

White, C.R., Alton, L.A., Crispin, T.S. & Halsey, L.G. (2016) Phylogenetic comparisons of pedestrian locomotion costs: confirmations and new insights. Ecology and Evolution,6,6712-6720.

Winwood-Smith, H.S., Franklin, C.E. & White, C.R. (2017) Low-carbohydrate diet induces metabolic depression: A possible mechanism to conserve glycogen. American Journal of Physiology – Regulatory Integrative and Comparative Physiology,313,R347-R356.