Annual Report 2019

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.

Directors’ message

In last year’s message I explained how, in 2018, some of the fundamental ideas that form the basis of the Centre for Geometric Biology were presented in publications. We began 2019 with a lively exchange between ourselves and international colleagues that resulted from one of these publications.  These discussions took place in the journal Trends in Evolutionary Ecology and we have included a summary in this report. Other discussions are ongoing with publications arising in the coming months. We also published some of our thinking about how incorporating energy use (metabolic theory) with life history theory can be combined to provide more generally applicable explanations of observations that neither theory can adequately explain on their own.

An important focus of the Centre is to demonstrate the applied value of the geometric theory of biology and in 2019 we published an important paper that details how we are underestimating the importance of Marine Protected Areas in fisheries management. This work, along with a separate study on the trophic footprint of marine infrastructure, was published in The Conversation allowing us to communicate our ideas to a far larger audience than the scientific community alone.

We continue to strive to publish high quality research in leading journals and in 2019 felt we succeeded. We frequently publish with international collaborators and have worked hard at strengthening these collaborations through conference attendance, invited talks, visiting labs overseas as well as hosting collaborators here at Monash.

One of our central areas of research has stemmed from the artificial selection of small and large algal cells which has now been ongoing for almost four years. This research allows us to disentangle the effects of size from potentially confounding factors such as age or species type, allowing tests of ecological and evolutionary theory that aren’t usually possible. We are excited at the research avenues that these algae have opened up for us and looking forward to further exploiting the possibilities they provide. These approaches have been expanded to a range of other burgeoning model species.

In 2020 we will continue to expand these core research areas in the field of geometric biology and begin the application process to become an Australian Research Council Centre of Excellence.

Work recently accepted in Nature Ecology & Evolution hints that 2020 will be our biggest year so far in terms of impactful publications.


Looking back: research highlights 2019

While choosing research highlights is never easy, we present research summaries, 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.

Debating growth and reproduction

In a recent post we described a paper written by Dustin Marshall and Craig White and published in Trends in Ecology and Evolution (TREE). The published article was called “Have we outgrown the existing models of growth?” In it, Dustin and Craig suggest that the growth dynamics that biologists have long sought to understand probably emerge simply from hyperallometric scaling of reproduction.

Daniel Pauly is a fisheries scientist from the University of British Columbia and is a proponent of the Gill-Oxygen Limitation Theory (GOLT) of growth. This theory applies to water-breathing animals and is structured around the proposition that growth is necessarily constrained by the size of the gills and the oxygen they are able to extract from the water.

Professor Pauly argues in a letter to TREE that there is a good reason why growth is not considered to be influenced by reproduction in the context of GOLT. While he agrees that reproductive output tends to scale hyperallometrically in fish, he does not agree that fish slow their growth because they allocate increasingly more to reproduction. Instead, he thinks that as growth slows (due to oxygen limitation caused by physical constraints on gill size) increased allocation of resources is directed to reproduction.

In their rebuttal, Dustin and Craig summarise their difference in opinion as one of causality; while Professor Pauly argues that body size in fish is limited by gill area, they believe that organs evolve to provide capacity to meet an organisms requirements. Or, in other words, the trait of body size is the product of selection whereby the size of an organisms is the best it can be to maximise fitness in a particular environment. Most importantly, taken to its logical extension, Dustin and Craig argue that Pauly’s own arguments imply fish reproduction should decrease with size.

In a separate letter, Michael Kearney from the University of Melbourne suggests that a radical revision of growth models is premature. In this case, Associate Professor Kearney suggests that a mechanistic modelling approach (such as Dynamic Energy Budget theory) based on a thermodynamically explicit theory of metabolism is better suited to understanding growth than the phenomenological modelling approach proposed by Dustin and Craig.

While Assoc. Prof. Kearney argues that the Dynamic Energy Budget model can incorporate hyperallometric scaling by adjusting the ‘rules’ governing how much energy is allocated to reproduction, Craig and Dustin say that to do this requires a phenomenological approach and is an unjustified post hoc model fitting solution. According to Craig and Dustin, this means that Assoc. Prof. Kearney’s model is not strictly mechanistic, with some parameters estimated by fitting mechanistic functions and some parameters requiring empirical data (a phenomenological approach).

But there is some agreement. Dustin, Craig and Michael Kearney are all interested in seeing studies of growth and metabolism that are conducted in the context of a full accounting of energy and mass balances (food in, changes in length and weight, respiration, faeces and eggs out) to continue improving our understanding of why organisms are the size they are.

Why do cooler mothers produce larger offspring?

In a recently published letter, Amanda Pettersen, Craig White, Rob Bryson-Richardson and Dustin Marshall propose a simple model to explain a pervasive conundrum – why do cooler mothers produce larger offspring?

Life history theory maintains that mothers balance the costs and benefits of making a few larger and better performing offspring against making many smaller and poorer performing offspring.

A major challenge to the theory is the fact that temperature seems to alter the optimisation of this trade off. Observations indicate that across a wide range of taxa and systems, mothers in warmer conditions produce smaller offspring. What is more, experimental studies have also shown that increasing temperatures decrease offspring size.

Amanda and her PhD supervisors are proposing that linking life history theory and metabolic theory, which relates to energy use, can provide a widely applicable explanation to the offspring size / temperature relationship.

Their model is centred on the cost of development. Mothers must provision their offspring until they are able to feed for themselves, that is, attain nutritional independence. The time spent in this developmental phase coupled with the energy expended will comprise the ‘cost’ of development. The minimum offspring size that allows individuals to reach nutritional independence must, then, increase with increasing cost of development.

As temperatures increase, developmental rate is expected to increase so that less time is spent in the developmental phase and metabolic rates (rates of energy use) are also expected to increase. The research team are suggesting that we consider how sensitive these two components are to temperature. If developmental rate is more sensitive to changes in temperature than metabolic rate, then the cost associated with provisioning offspring to achieve nutritional independence will decrease with increasing temperatures.

Or to put it another way, if developmental rate increases more than metabolic rate as temperatures rise, so that the developmental time is shorter in relation to metabolic rate, then the developmental cost is lower and offspring are smaller at higher temperatures. If, however, metabolic rate is more sensitive to changing temperatures than developmental rate then the converse is true; the developmental cost will increase with increasing temperatures and offspring are predicted to be larger at higher temperatures.

In order to develop and test these ideas the team needed to generate measures of temperature dependence of metabolic rate and developmental rate simultaneously, something that hadn’t been done before in a systematic fashion.

They started by methodically searching published literature to determine the relationship between the temperature that mothers experience and the size of their offspring. They then experimentally manipulated temperature to examine how developmental rate and metabolic rates changed in two very different species – the bryozoan Bugula neritinaand the zebrafish Danio rerio. They used the data from these experiments to develop the mathematical functions for their model to determine how the costs of development change with temperature. Finally they searched the literature again to get data on the temperature dependence of developmental and metabolic rates for a wide range of species because they wanted to test whether their model could apply more generally.

Amanda and her colleagues found that the offspring size / temperature relationship is widespread.  Also in the two species they collected experimental data for, they found that development time is more sensitive to temperature than metabolic rates. This means that the overall costs of development decrease with temperature. What is more, they found that this pattern applies more broadly – for 72 species across five phyla the costs of development are higher at cooler temperatures.

Combining life history theory and metabolic theory has allowed In a recently published letter, Amanda Pettersen, Craig White, Rob Bryson-Richardson and Dustin Marshall propose a simple model to explain a pervasive conundrum – why do cooler mothers produce larger offspring?

Life history theory maintains that mothers balance the costs and benefits of making a few larger and better performing offspring against making many smaller and poorer performing offspring.

A major challenge to the theory is the fact that temperature seems to alter the optimisation of this trade off. Observations indicate that across a wide range of taxa and systems, mothers in warmer conditions produce smaller offspring. What is more, experimental studies have also shown that increasing temperatures decrease offspring size.

Amanda and her PhD supervisors are proposing that linking life history theory and metabolic theory, which relates to energy use, can provide a widely applicable explanation to the offspring size / temperature relationship.

Their model is centred on the cost of development. Mothers must provision their offspring until they are able to feed for themselves, that is, attain nutritional independence. The time spent in this developmental phase coupled with the energy expended will comprise the ‘cost’ of development. The minimum offspring size that allows individuals to reach nutritional independence must, then, increase with increasing cost of development.

As temperatures increase, developmental rate is expected to increase so that less time is spent in the developmental phase and metabolic rates (rates of energy use) are also expected to increase. The research team are suggesting that we consider how sensitive these two components are to temperature. If developmental rate is more sensitive to changes in temperature than metabolic rate, then the cost associated with provisioning offspring to achieve nutritional independence will decrease with increasing temperatures.

Or to put it another way, if developmental rate increases more than metabolic rate as temperatures rise, so that the developmental time is shorter in relation to metabolic rate, then the developmental cost is lower and offspring are smaller at higher temperatures. If, however, metabolic rate is more sensitive to changing temperatures than developmental rate then the converse is true; the developmental cost will increase with increasing temperatures and offspring are predicted to be larger at higher temperatures.

In order to develop and test these ideas the team needed to generate measures of temperature dependence of metabolic rate and developmental rate simultaneously, something that hadn’t been done before in a systematic fashion.

They started by methodically searching published literature to determine the relationship between the temperature that mothers experience and the size of their offspring. They then experimentally manipulated temperature to examine how developmental rate and metabolic rates changed in two very different species – the bryozoan Bugula neritinaand the zebrafish Danio rerio. They used the data from these experiments to develop the mathematical functions for their model to determine how the costs of development change with temperature. Finally they searched the literature again to get data on the temperature dependence of the research team to provide a general explanation for offspring size / temperature relationships. In colder temperatures mothers show an adaptive response whereby they offset the increased costs of development by making larger offspring that possess greater energy reserves.

This figure shows the relationship between two biological rates; development time (D) and metabolic rate (MR). In the top graph we can see that as temperature increases from T4 to T1, development time is expected to decrease and Metabolic Rate is expected to increase. The bottom panels demonstrate what is predicted to happen when b) the developmental rate is more sensitive to temperature than metabolic rate and so c) the total costs of development (and therefore offspring size) should decrease with increasing temperature. In d) the converse is true – metabolic rate is more sensitive to temperature than developmental rate and so e) total costs of development (and offspring size) will increase with increasing temperature.

How can pathogens optimise both transmission and dispersal?

Certain pathogens (disease-producing organisms) are stuck in a Catch-22; to survive they need to continue to find, and infect, new hosts. But infection makes their hosts sick and less likely to move to where there are new hosts to infect.

PhD student Louise Nørgaard and her supervisors Ben Phillips and Matt Hall have found evidence of a pathogen that resolves this issue by exploiting the differences in size and behaviour of male and female hosts to optimize its own chance of successful infection.

The team uses the freshwater crustacean Daphnia magna and its common pathogen Pasteuria ramosa as a model system to test the idea that a pathogen can exploit differences between the sexes of a host to its advantage. The pathogen P. ramosa is ingested by Daphnia after which it sterilises and kills the host, releasing transmission spores that are ready to infect a new host. Female Daphnia are bigger, live longer and are more susceptible to infection than males.

Louise set up two separate experiments, allowing her to monitor the probability that Daphnia would disperse from a crowded area to a less crowded area and to measure the rate and distance travelled by infected and uninfected male and female individuals.

In the first experiment Louise was able to capitalise on previous work that has shown that Daphnia will disperse when conditions are crowded. Exposure to water taken from high densities of Daphniais enough to encourage dispersal. Louise used ‘crowded-conditioned’ water and found infected male Daphnia were more likely to disperse than uninfected males. Infected females, on the other hand, were a lot less likely to disperse than uninfected females.

A second experiment found that infected females had four times the number of transmission spores than infected males and moved less far and more slowly than males or uninfected females. Infected males though, moved at the same rate and travelled the same distance as uninfected males.

The figure (a) shows how far male (blue) and females (green) disperse when infected with the pathogen compared to uninfected individuals. Louise tested two types of pathogen C1 and C19. She also measured the distance travelled (b) and the spore load in infected individuals (c).

So how do these differences between the sexes help the pathogen? Females are bigger and can host large numbers of transmission spores. Staying put when densities are high means they are releasing this large number of spores into a crowd – potentially maximising the chance of further infections.  Smaller males have fewer spores to release and the chance of secondary infections may be maximised when they move to new areas where few individuals are already infected.

Importantly the differences in dispersal behaviour between infected males and females seem to relate directly to the way the pathogen interacts with each sex. Uninfected males and females had similar rates and distance of dispersal while uninfected females were more likely to move away from crowded habitats than males. These patterns disappear when both sexes are infected.

Do these different infection strategies in different sexes provide a form of bet-hedging for the pathogen? Louise and her supervisors think they do and, if widespread, will have important implications for disease dynamics.

Are we undervaluing the contribution of marine protected areas to fisheries?

Our recent research has found that we are systematically underestimating the true value of marine protected areas (MPAs) to fisheries.

An important function of MPAs is to protect both representative and unique ecological communities, but scientists have long hoped they can play another role: contributing to the replenishment and maintenance of exploited fish stocks.

Wild fisheries are under intense pressure and landings of fish catches have flattened out despite an ever-increasing fishing effort. The most effective kind of MPAs are areas we set aside as ‘no take’ zones, where removal of animals and plants is banned. Fish populations within these areas can grow with limited human interference and potentially ‘spill-over’ to replenish fished stocks outside of MPAs. Despite the potential benefit, anglers remain sceptical that any spill-over will offset the loss of fishing grounds and the role of MPAs in fisheries remains contentious.

When we calculate how much a protected area contributes to a fishery, we work out the average length of both fished and unfished populations. Fish inside MPAs are bigger, on average, than those outside and so will produce more offspring than their smaller relatives outside MPAs. Generally, fisheries scientists relate the size of the fish to the reproductive output, whereby one unit increase in size equates to one unit increase in egg production.  They estimate how many juveniles will ‘spill-over’ and enter the fishing grounds.

It turns out there are a number of problems with the way the spill-over effect is currently calculated. Length is generally the measure of fish size recorded in a survey, but focusing on length risks underestimating the differences in reproduction inside and outside of MPAs.  Length and mass do not change at the same rate, so a 28% increase in fish length results in a 109% increase in mass. It can seem counter-intuitive that increasing fish length by around one quarter more than doubles the mass because the human brain tends to struggle when thinking about non-linear relationships.

This is compounded when we consider another non-linear relationship; fish mass and reproductive output. Our research team from the Centre for Geometric Biology and collaborator Ross Robertson from the Smithsonian Tropical Research Institute, recently found that bigger fish produce disproportionately more eggs than smaller fish in all fish species they looked at. This research made us realise that we need to be focused on protecting the biggest fish in a fishery.

And that is not all. In 1906, Danish mathematician Johan Jensen described the ‘fallacy of the average’, now known as Jensen’s inequality. Jensen pointed out that when relationships are non-linear we can’t assume that the average performance is equal to the performance under average conditions.

In our example, Jensen’s inequality means we further under-estimate reproductive output from inside the MPA. This is because fish size relates to reproductive output in a non-linear way so the reproductive output at average size is not the same as the average reproductive output. The inequality is greater inside the MPA where fish sizes are bigger and so this makes a further contribution to our under-estimate of reproductive output.

Jensen’s inequality for fish reproduction. (a) The benefit of MPAs for average fish reproduction driven by differences in mean size. (b) The benefits of MPAs are enhanced because of the greater ‘inequality’ in the MPAs where fish sizes are larger and more variable.

When we take Jensen’s inequality into account, and add it to the underestimates relating to the non-linear relationships already discussed, we find that there is a 175% increase in reproductive output for fish inside MPAs compared to those outside.

While this translates to a much smaller ‘spill-over’ effect, (more like a 12% increase in tonnes of caught fish per year for the coral trout fishery when MPAs are included in the management of the fishery), it is still a substantial increase in yield.

Jensen’s inequality for fish reproduction: the benefit of MPAs for average fish reproduction driven by differences in mean size. (b) The benefits of MPAs are enhanced because of the greater ‘inequality’ in the MPAs where fish sizes are larger and more variable.
Overall benefits of MPAs when we re-calculate total reproduction accounting for non-linear relationships between length and mass and mass and reproduction. Yellow bars show length, mass, and reproductive output of fish of average size outside the protected area; blue bars show length, mass, and reproductive output of fish inside protected areas.

MPAs represent an essential tool for protecting larger fish, and the research team hope that a more accurate accounting of the value of MPAs will increase support for their use by a wide variety of stakeholders, including anglers themselves.

This work was also published in The Conversation.


Ongoing work

There are a number of projects that will continue to be a core part of generating data to test the Theory of Geometric Biology as well as testing other established ecological and evolutionary theories. One of these is the artificial selection of large and small algal cells that has been ongoing for almost 4 years now. Researchers have also been looking at the relationship between size and reproductive output and over that same 3-4 year time period have been laboriously amassing data into a database to allow them to test whether bigger individuals produce disproportionally more gametes in a wide range of species.

500 generations of experimental evolution

Three and a half years ago Martino Malerba set up the first culture of the single celled marine phytoplankton Dunaliella tertiolecta and begun to artificially select for large and small cells.  The selection process of separating the largest and the smallest cells has continued twice a week ever since.  Martino is now the proud ‘father’ of algal cells where the big cells are more than 10 times the size of the smaller cells.

The evolved algae lines have enabled Martino and his colleagues to look at the consequences of being a particular size without having to compare different species, which vary in many other ways than just size.  This research directly supports the fundamental question the Centre for Geometric Biology seeks to understand “why do organisms grow to the size they do?”

The team has looked at the effects of size at both the level of the cell and the population.  They have found that altering the size of a cell profoundly alters many fundamental traits of algal physiology and ecology.  This affects how cells of different sizes will cope with fluctuating resources and, in turn, how those populations of cells use energy and grow.

Exciting research underway looks at community level effects.  What happens when grazers are only offered either large or small algal cells: does changing algal size have repercussions up the food chain?

Understanding how individuals grow and regulate their energy is critical in helping scientists predict how large-scale impacts, such as climate change, affect organisms.

Phytoplankton have critical roles in the ocean; they form the base of most food webs and fix large amounts of carbon.  So, while the research stemming from these artificially evolved algal cells is theoretically interesting, it also has a very direct and immediate application to how we understand and manage climate change.

Size and reproduction; compiling a database

In 2018 the we published a number of papers that addressed a core area of research for the Centre. These papers considered the relationship between size and reproductive output and what that meant for our understanding of patterns of growth.

In order to do this, researchers compiled a database that accessed published work from the last 100 years that included data on fish size and reproductive output. When they examined the data from 342 species of fish they found that there was a hyper-allometric relationship between size and reproductive output in 95% of the species they looked at.

This information has massive repercussions for the way in which we manage our fisheries but also, if it is a more general rule, it may change the way we understand growth.

So, is it a more general rule – do larger individuals produce disproportionately more gametes / offspring than smaller individuals in taxa other than fish?

Michaela Parascandalo joined the team towards the end of 2018 to focus on gathering data to address this question. Initially she searched for data on invertebrates but has since expanded her search to include a total of 10 phyla. Michaela uses Google Scholar as the search engine and inputs a range of search terms that relate to body size and reproductive output. For each query entered, she looks at every paper displayed on the first 6 pages of results.  She is looking for graphs of length/mass and reproductive output.

Michaela will then open the graph in Data Thief, a program that allows you to extract datapoints from a picture of a graph.  In some cases, she has to do additional searches to get a conversion of length to mass for that species and latitudes and longitudes for the study.

All this information is entered into the database – the master copy has only one example of each species while the ‘duplicates’ file stores data from overlapping species’ that might be from different times or locations.

So far there are 75,000 data points in the master file, 30,000 data points in the duplicates file, 10 phyla, 978 species, a data span of 92 years and Michaela has repeatedly been identified as a ‘bot’.

The Centre for Geometric Biology is collating data to enable them to ask if larger individuals produce disproportionately more gametes / offspring than smaller individuals in taxa other than fish? Photo source: Alligator – Pixabay. Centipede – Wikipedia Commons.

There is more to do, but once Michaela has finished compiling the data, the team will be in a good position to assess the generality of hyperallometry in species other than fish.  Do species such as alligator and centipedes shown above also exhibit hyperallometry?  They will also be able to use the ‘duplicate’ database look at how relationships between size and reproductive output vary through space and time.


CGB quickview

Publications
103
scientific publications since CGB began in 2015
30
publications from the CGB in 2019
90%
publications in top 10% journals by Cite Score in 2019
670
citations received by publications 2015-2019
47%
publications with international collaborators in 2019

Stats from Scopus and SciVal 21 January 2020 based on 103 publications identified by Scopus

Communications
38
posts published on website in 2019
4,435
website visitors in 2019
8
national and international media interviews
2
articles published in The Conversation with a combined total of 29,413 readers and 21 publishers*

*Source: The Conversation Dashboard 26 January 2020

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
5
international visitors hosted
2
Australian visitors hosted
2
CGB discussion groups including one mini symposium
5
work experience students hosted
1
writing retreat for leaders

Staff news

There have been a few changes in the core staff who are directly funded by the CGB.  Martino Malerba and Mariana Álvarez-Noreiga remain in the Centre as post-docs. Giulia Ghedini has also stayed within the Centre but is working under her own DECRA funding. Melissa Verrin who was based in Toronto and working with Troy Day at Queens University has decided to move on and returned to Europe. Hayley Cameron has completed her PhD and begun a years post-doc within the Centre and we are expecting another post-doc to begin early in 2020. Tormey Reimer, the Centre RA has also moved on and we are pleased to welcome Melanie Lovass to the CGB.

The management committee, Dustin Marshall and Craig White, remain and are primary supervisors to eight PhD students. Evatt Chirgwin and Hayley Cameron, were both awarded their PhDs in 2019.


Full list of publications

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(3) 653-661

Arnold, P.A., Rafter, M.A., Malekpour, R. and 3 more (…) (2017).Investigating movement in the laboratory: dispersal apparatus designs and the red flour beetle, Tribolium castaneum. Entomologia Experimentalis et Applicata,163(1) 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(6) 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(8) 890-898

Barneche, D.R., Ross Robertson, D., White, C.R. and 1 more (…) (2018).Fish reproductive-energy output increases disproportionately with body size. Science,360(6389) 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(1) 103-111

Bay, S., Ferrari, B., Greening, C. (2018).Life without water: How do bacteria generate biomass in desert ecosystems?. Microbiology Australia,39(1) 28-32

Bender, M.G., Leprieur, F., Mouillot, D. and 6 more (…) (2017).Isolation drives taxonomic and functional nestedness in tropical reef fish faunas. Ecography,40(3) 425-435

Bywater, C.L., Wilson, R.S., Monro, K. and 1 more (…) (2018).Legs of male fiddler crabs evolved to compensate for claw exaggeration and enhance claw functionality during waving displays. Evolution,72(11) 2491-2502

Cameron, H., Coulson, T., Marshall, D.J. (2019).Size and density mediate transitions between competition and facilitation. Ecology Letters,22(11) 1879-1888

Cameron, H., Marshall, D.J. (2019).Can competitive asymmetries maintain offspring size variation? A manipulative field test. Evolution,73(8) 1663-1671

Cameron, H., Monro, K., Malerba, M. and 2 more (…) (2016).Why do larger mothers produce larger offspring? A test of classic theory. Ecology,97(12) 3452-3459

Cameron, H., Monro, K., Marshall, D.J. (2017).Should mothers provision their offspring equally? A manipulative field test. Ecology Letters,20(8) 1025-1033

Cantor, M., Pires, M.M., Marquitti, F.M.D. and 10 more (…) (2017).Nestedness across biological scales. PLoS ONE,12(2)

Carere, C.R., Hards, K., Houghton, K.M. and 9 more (…) (2017).Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME Journal,11(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(22) 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(2)

Chirgwin, E., Marshall, D.J., Monro, K. (2019).Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Functional Ecology,

Chirgwin, E., Marshall, D.J., Sgrò, C.M. and 1 more (…) (2017).The other 96%: Can neglected sources of fitness variation

offer new insights into adaptation to global change?. Evolutionary Applications,10(3) 267-275

Chirgwin, E., Marshall, D.J., Sgrò, C.M. and 1 more (…) (2018).How does parental environment influence the potential for adaptation to global change?. Proceedings of the Royal Society B: Biological Sciences,285(1886)
Connallon, T., Chenoweth, S.F. (2019).Dominance reversals and the maintenance of genetic variation for fitness. PLoS Biology,17(1)

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(1) 65-87

Connallon, T., Olito, C., Dutoit, L. and 3 more (…) (2018).Local adaptation and the evolution of inversions on sex chromosomes and autosomes. Philosophical Transactions of the Royal Society B: Biological Sciences,373(1757)

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(1) 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(11) 2251-2256

Dong, X., Greening, C., Brüls, T. and 7 more (…) (2018).Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats. ISME Journal,12(8) 2039-2050

Dubuc, A., Waltham, N., Malerba, M. and 1 more (…) (2017).Extreme dissolved oxygen variability in urbanised tropical wetlands: The need for detailed monitoring to protect nursery ground values. Estuarine, Coastal and Shelf Science, 198163-171

Dunn, R.E., White, C.R., Green, J.A. (2018).A model to estimate seabird field metabolic rates. Biology Letters,14(6)

Ghedini, G., Connell, S.D. (2017).Moving ocean acidification research beyond a simple science: Investigating ecological change and their stabilizers. Food Webs,1353-59

Ghedini, G., Loreau, M., White, C.R. and 1 more (…) (2018).Testing MacArthur’s minimisation principle: do communities minimise energy wastage during succession?. Ecology Letters,21(8) 1182-1190

Ghedini, G., White, C.R., Marshall, D.J. (2017).Does energy flux predict density-dependence? An empirical field test. Ecology,98(12) 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(6) 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(3) 428-437

Gipson, S.A.Y., Jimenez, L., Hall, M.D. (2019).Host sexual dimorphism affects the outcome of within-host pathogen competition. Evolution,73(7) 1443-1455

Good, B.H., McDonald, M.J., Barrick, J.E. and 2 more (…) (2017).The dynamics of molecular evolution over 60,000 generations. Nature,551(7678) 45-50

Grémillet, D., White, C.R., Authier, M. and 3 more (…) (2017).Ocean sunfish as indicators for the ‘rise of slime’. Current Biology,27(23) R1263-R1264

Hachich, N.F., Bonsall, M.B., Arraut, E.M. and 3 more (…) (2016).Marine island biogeography. Response to comment on ‘Island biogeography: patterns of marine shallow-water organisms’. Journal of Biogeography,43(12) 2517-2519

Hall, M.D., Mideo, N. (2018).Linking sex differences to the evolution of infectious disease life-histories. Philosophical Transactions of the Royal Society B: Biological Sciences,373(1757)

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(2) 161-166

Halsey, L.G., White, C.R. (2019).Terrestrial locomotion energy costs vary considerably between species: no evidence that this is explained by rate of leg force production or ecology. Scientific Reports,9(1)

Hangartner, S., Lasne, C., Sgrò, C.M. and 2 more (…) (2019).Genetic covariances promote climatic adaptation in Australian Drosophila. Evolution, Hector, T.E., Sgrò, C.M., Hall, M.D. (2019).Pathogen exposure disrupts an organism’s ability to cope with thermal stress. Global Change Biology,25(11) 3893-3905

Ji, M., Greening, C., Vanwonterghem, I. and 11 more (…) (2017).Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature,552(7685) 400-403

Lagos, M.E., Barneche, D.R., White, C.R. and 1 more (…) (2017).Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions. Global Change Biology,23(6) 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(6) 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(11) 2080-2086

Lange, R., Marshall, D. (2017).Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Scientific Reports,7(1)

Lange, R., Monro, K., Marshall, D.J. (2016).Environment-dependent variation in selection on life history across small spatial scales. Evolution,70(10) 2404-2410

Lawson, C.L., Halsey, L.G., Hays, G.C. and 5 more (…) (2019).Powering Ocean Giants: The Energetics of Shark and Ray Megafauna. Trends in Ecology and Evolution,34(11) 1009-1021

Lawton, R.J., Paul, N.A., Marshall, D.J. and 1 more (…) (2017).Limited evolutionary responses to harvesting regime in the intensive production of algae. Journal of Applied Phycology,29(3) 1449-1459

Liedke, A.M.R., Barneche, D.R., Ferreira, C.E.L. and 7 more (…) (2016).Abundance, diet, foraging and nutritional condition of the banded butterflyfish (Chaetodon striatus) along the western Atlantic. Marine Biology,163(1) 1-13

Malerba, M.E., Marshall, D.J. (2019).Size-abundance rules? Evolution changes scaling relationships between size, metabolism and demography. Ecology Letters,22(9) 1407-1416

Malerba, M.E., Marshall, D.J. (2020).Testing the drivers of the temperature–size covariance using artificial selection. Evolution,74(1) 169-178

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(1884)

Malerba, M.E., Palacios, M.M., Palacios Delgado, Y.M. and 2 more (…) (2018).Cell size, photosynthesis and the package effect: an artificial selection approach. New Phytologist,219(1) 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(12) 3106-3115

Malerba, M.E., White, C.R., Marshall, D.J. (2018).Eco-energetic consequences of evolutionary shifts in body size. Ecology Letters,21(1) 54-62

Malerba, M.E., White, C.R., Marshall, D.J. (2019).The outsized trophic footprint of marine urbanization. Frontiers in Ecology and the Environment,17(7) 400-406

Maliha, M., Herdman, M., Brammananth, R. and 5 more (…) (2020).Bismuth phosphinate incorporated nanocellulose sheets with antimicrobial and barrier properties for packaging applications. Journal of Cleaner Production,246

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

Marshall, D.J., Gaines, S., Warner, R. and 2 more (…) (2019).Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and the Environment,17(7) 407-413

Marshall, D.J., Lawton, R.J., Monro, K. and 1 more (…) (2018).Biochemical evolution in response to intensive harvesting in algae: Evolution of quality and quantity. Evolutionary Applications,11(8) 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(6) 1436-1446

Marshall, D.J., White, C.R. (2019).Aquatic Life History Trajectories Are Shaped by Selection, Not Oxygen Limitation. Trends in Ecology and Evolution,34(3) 182-184

Marshall, D.J., White, C.R. (2019).Have We Outgrown the Existing Models of Growth? Trends in Ecology and Evolution,34(2) 102-111

Matthews, G., Hangartner, S., Chapple, D.G. and 1 more (…) (2019). Quantifying maladaptation during the evolution of sexual dimorphism. Proceedings of the Royal Society B: Biological Sciences, 286(1908)

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(1834)

Morrissey, M.B., Hangartner, S., Monro, K. (2019).A note on simulating null distributions for G matrix comparisons. Evolution,73(12) 2512-2517

Nang, S.C., Morris, F.C., McDonald, M.J. and 5 more (…) (2018).Fitness cost of mcr-1-mediated polymyxin resistance in Klebsiella pneumoniae. Journal of Antimicrobial Chemotherapy,73(6) 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(4) 518-524

Nørgaard, L.S., Phillips, B.L., Hall, M.D. (2019).Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?. Biology Letters,15(6)

Ohmer, M.E.B., Cramp, R.L., Russo, C.J.M. and 2 more (…) (2017).Skin sloughing in susceptible and resistant amphibians regulates infection with a fungal pathogen. Scientific Reports,7(1)

Ohmer, M.E.B., Cramp, R.L., White, C.R. and 7 more (…) (2019).Phylogenetic investigation of skin sloughing rates in frogs: Relationships with skin characteristics and disease-driven declines. Proceedings of the Royal Society B: Biological Sciences,286(1896)

Olito, C. (2017).Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites. Evolution,71(2) 458-464

Olito, C., Abbott, J.K., Jordan, C.Y. (2018).The interaction between sex-specific selection and local adaptation in species without separate sexes. Philosophical Transactions of the Royal Society B: Biological Sciences,373(1757)

Olito, C., Connallon, T. (2019).Correction: Sexually Antagonistic Variation and the Evolution of Dimorphic Sexual Systems” by Colin Olito and Tim Connallon (American Naturalist, (2019), 193, (688-701)). American Naturalist,194(5) 741-742

Olito, C., Connallon, T. (2019).Sexually antagonistic variation and the evolution of dimorphic sexual systems. American Naturalist,193(5) 688-701

Olito, C., Marshall, D.J. (2019).Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae). Journal of Evolutionary Biology,32(2) 177-186

Olito, C., White, C.R., Marshall, D.J. and 1 more (…) (2017).Estimating monotonic rates from biological datausing local linear regression. Journal of Experimental Biology,220(5) 759-764

Pettersen, A.K., Marshall, D.J., White, C.R. (2018).Understanding variation in metabolic rate. Journal of Experimental Biology,221(1)

Pettersen, A.K., White, C.R., Bryson-Richardson, R.J. and 1 more (…) (2018).Does the cost of development scale allometrically with offspring size?. Functional Ecology,32(3) 762-772

Pettersen, A.K., White, C.R., Bryson-Richardson, R.J. and 1 more (…) (2019).Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters,22(3) 518-526

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(1831)

Polymeropoulos, E.T., Oelkrug, R., White, C.R. and 1 more (…) (2017).Phylogenetic analysis of the allometry of metabolic rate and mitochondrial basal proton leak. Journal of Thermal Biology,6883-88

Portugal, S.J., Ricketts, R.L., Chappell, J. and 3 more (…) (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(1727)

Portugal, S.J., Sivess, L., Martin, G.R. and 2 more (…) (2017).Perch height predicts dominance rank in birds. Ibis,159(2) 456-462

Portugal, S.J., White, C.R., Frappell, P.B. and 2 more (…) (2019).Impacts of “supermoon” events on the physiology of a wild bird. Ecology and Evolution,9(14) 7974-7984

Prokopuk, L., Stringer, J.M., White, C.R. and 5 more (…) (2018).Loss of maternal EED results in postnatal overgrowth. Clinical Epigenetics,10(1) Reference

Rooney, W.M., Grinter, R.W., Correia, A. and 3 more (…) (2019).Engineering bacteriocin-mediated resistance against the plant pathogen Pseudomonas syringae. Plant Biotechnology Journal,

Schuster, L., White, C.R., Marshall, D.J. (2019).Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate. Invertebrate Biology,138(1) 55-66

Seymour, R.S., Hu, Q., Snelling, E.P. and 1 more (…) (2019).Interspecific scaling of blood flow rates and arterial sizes in mammals. Journal of Experimental Biology,222(7)

Sezmis, A.L., Malerba, M.E., Marshall, D.J. and 1 more (…) (2018).Beneficial Mutations from Evolution Experiments Increase Rates of Growth and Fermentation. Journal of Molecular Evolution,86(2) 111-117

Svanfeldt, K., Monro, K., Marshall, D.J. (2017).Dispersal duration mediates selection on offspring size. Oikos,126(4) 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(3) 654-661

Svanfeldt, K., Monro, K., Marshall, D.J. (2018).Resources mediate selection on module longevity in the field. Journal of Evolutionary Biology,31(11) 1666-1674

Tate, M., McGoran, R.E., White, C.R. and 1 more (…) (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(3) 723-749

Uesugi, A., Connallon, T., Kessler, A. and 1 more (…) (2017).Relaxation of herbivore-mediated selection drives the evolution of genetic covariances between plant competitive and defense traits. Evolution,71(6) 1700-1709

Wannier, T.M., Kunjapur, A.M., Rice, D.P. and 3 more (…) (2018).Adaptive evolution of genomically recoded Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America,115(12) 3090-3095

White, C.R., Alton, L.A., Crispin, T.S. and 1 more (…) (2016).Phylogenetic comparisons of pedestrian locomotion costs: confirmations and new insights. Ecology and Evolution,6(18) 6712-6720

White, C.R., Marshall, D.J. (2019).Should We Care If Models Are Phenomenological or Mechanistic? Trends in Ecology and Evolution,34(4) 276-278

White, C.R., Marshall, D.J., Alton, L.A. and 15 more (…) (2019).The origin and maintenance of metabolic allometry in animals. Nature Ecology and Evolution,3(4) 598-603

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(4) R347-R356

Winwood-Smith, H.S., White, C.R. (2018).Short-duration respirometry underestimates metabolic rate for discontinuous breathers. The Journal of experimental biology,221