Mirth recognised with Crozier medal

The Centre for Geometric Biology’s Christen Mirth has been recognised for her research on how nutrition shapes development, having been awarded the Ross Crozier medal by the Genetics Society of Australasia.

When Christen first began working on this problem in 2003, using the fruit fly Drosophila melangoster as a model, researchers knew that nutrition had a role in the secretion of insulin-like peptides. These peptides, in turn, influenced the rates of body growth.  What they didn’t know, was what made insects stop growing.

During her postdoc, Christen and her colleagues discovered there was another hormone involved in regulating when growth should stop: ecdysone, the steroid that controls moulting in insects. It turned out that nutritional changes can control the timing of a critical pulse of ecdysone, which commits an insect to metamorphosis. In other words, ecdysone was the key they had been looking for, determining the developmental rate and the final size of the insect.

What’s more, the team found certain organs, such as the wings and the ovaries, require this ecdysone pulse for cells to acquire organ-specific identities and to grow. Organs also change the way they respond to nutritional cues with time by changing the combination of hormones required for growth, providing a further buffer against nutritional environments determining organ size. Such differences in the way organs respond to nutrition (and the associated hormone releases) are important as they allow for variation in animal shape and ensure that correct organ function is maintained in different nutritional conditions.

Christen has gone on to investigate other hormones and, in collaboration with colleague Associate Professor Alexander Shingleton of the University of Illinois, has found another developmental hormone that regulates body size but not developmental timing. This ‘juvenile hormone’ reduces insulin signalling and increases the concentration of ecdysone without altering the timing of ecdysone pulses.

Now as leader of the Mirth Lab, Christen emphasises how the group’s work provides a theory for the way nutrition might influence the growth of other animals. Nutrition may act as a stimulus, modifying insulin signalling and the synthesis of key developmental hormones like sex steroids in mammals.

The Ross Crozier medal was established by the Genetics Society of Australasia to recognise outstanding contributions to the field of genetics research by mid-career Australasian scientists. It has been awarded annually since 2011. The medal commemorates celebrated Australian evolutionary geneticist Ross Crozier (1943–2009).

The benefits of big neighbours

Larger offspring typically have higher survival, growth and reproduction than smaller offspring. So why then, do we see such a range in offspring size? PhD student Hayley Cameron tackles this conundrum and the results of her latest experimental study contradict accepted theoretical models by showing that bigger is not always better.

Classic life-history models assume a trade-off in the investment mothers make in the next generation; large offspring perform better but smaller offspring are ‘cheaper’ to make and so mothers make them in large numbers. These models predict that a single offspring size will maximise reproductive success in a particular environment. But, we don’t see single offspring sizes, we see a range of sizes.

Game-theory takes the models further and explains the variation in offspring size by generating a ‘competition-colonisation’ trade-off.  In these scenarios, larger offspring will win contests over smaller offspring, but smaller offspring are better able to colonise unoccupied areas because they are more abundant. This means, no single offspring size will maximise reproductive success for any given population and so variation in offspring size is maintained.

Hayley and her supervisor Dustin Marshall test the idea that larger offspring will out-compete smaller offspring in a well-studied model organism, the invertebrate Bugula neritina. This idea has received surprisingly little testing.

To do this Hayley collected larvae and measured each one before settling them on to acetate squares. She glued these acetate squares, with their newly settled offspring, onto PVC plates in pairs of different sizes. These plates were deployed at a field site and every week Hayley measured survival, growth and number of developing larvae for 336 individuals of known offspring size.

To their surprise Hayley and Dustin found, instead of being out-competed as predicted, small offspring received benefits from having larger offspring as neighbours. Large offspring did compete with large neighbours though, and these bigger offspring did best on their own.

The graph and table both show how reproduction (measured by the number of ovicells) in big and small Bugula changed depending on the size of its neighbour. Hayley found that when small Bugula were paired with big neighbours then the overall reproductive output of the small Bugula increased. In contrast, big Bugula did best with no neighbours at all.

Why did this happen? In this study, larger offspring grew into larger colonies and Hayley and Dustin think these larger colonies disrupt the flow which affects the supply of resources (food and oxygen) available to their neighbours.  A slower flow is likely to benefit smaller colonies which tend to be less efficient at capturing resources in high flows. Conversely, larger, more efficient, colonies may deplete the resources available for their large neighbours.

So, while life history theory has traditionally viewed offspring interactions through the lens of competition, Hayley’s PhD work suggests facilitation might also be important in maintaining variation in offspring size.

More of Hayley’s PhD work on variation in offspring size: Should mothers provision their offspring equally? A manipulative field test

This research is published in the journal Evolution.

Celebrating 500 generations of experimental evolution

It’s party time in the Centre for Geometric Biology: We’ve reached 500 generations of experimental evolution in our large and small algal cells!

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.

Estimating the effects of marine urbanization on coastal food webs

Marine urbanization is a term that describes the increasing proliferation of structures such as piers, jetties, marinas, sea walls and other coastal defences in the marine environment. Martino Malerba, Craig White and Dustin Marshall from the Centre for Geometric Biology are proposing that this type of urban spread into the ocean could rob local systems of some of their productivity, changing local food web structure as well as function.

Many artificial structures, including floating platforms, barges, piers, pontoons seawalls and port quays, decrease the access of direct sunlight into the water. This means that instead of ecological communities dominated by ‘energy-producing’ seaweeds that require light to photosynthesise, there tends to be a shift toward dense assemblages of ‘energy-consuming’ filter-feeding invertebrates. The research team are particularly interested in finding out how this additional filter-feeding biomass affects energy flow and the productivity of coastal food webs.

The sheltered and shaded nature of marine urbanization disproportionately favours the development of dense fouling invertebrate communities. Examples of marine artificial structures in Australia: (left panel) mussels in the port of Hobart, (right top) mixed fouling communities in Port Phillip Bay, and (right bottom) colonies of mussels and polychaetes in Brighton (Melbourne).

Martino and his colleagues have combined data from field surveys, laboratory studies and satellite data to analyse total energy usage of invertebrate communities on artificial structures in Port Phillip and Moreton Bays. The team then used estimates from other studies to estimate the amount of primary production required to support the metabolic demands of the entire filter-feeding biomass living on artificial structures of all main commercial ports worldwide: the ‘trophic footprint’.

In order to do this, Martino and colleagues first used satellite photos to estimate how much area available for colonisation is created by artificial structures in Port Phillip and Moreton Bays. They then used field surveys to estimate the total invertebrate biomass occurring on all artificial structures in the two bays. In Port Phillip Bay, the estimated biomass on artificial structures is the equivalent of 3,151 female African bush elephants.

The next step was to transport communities back to the laboratory to measure mean daily energy consumption per unit area and then scale this up to artificial structures within the whole bay.  Based on their estimates they found that biomass on artificial structures can consume between 0.005% and 0.05% of the total yearly energy production in Port Phillip Bay and Morton Bay respectively.  This means that each square metre of artificial structure will consume 6 to 20 m² of marine primary productivity in these bays.

When they went through essentially the same process using data available from the scientific literature, the team found, on average, each metre of port consumes 26 m²of ocean primary productivity.  But there are stark differences between ports in different parts of the world. For example, one square metre of artificial structure in cold, highly productive regions can require as little as 0.9 m² of ocean (e.g. St. Petersburg, Russia), whereas a square metre of artificial structure in the nutrient-poor tropical waters of Hawaii can deplete all of the productivity in the surrounding ~120 m².

Distribution of all major commercial ports worldwide, with associated area of underwater artificial structures (size of grey dot) and trophic footprint (size of red border). Trophic footprints indicate how much ocean surface is required to supply the energy demand of the sessile fouling community growing on all artificial structures of the port, averaged over the year. Trophic footprints depend on local conditions of ocean primary productivity and temperature. Ports located in cold, nutrient-rich waters (dark blue) will have a lower footprint than ports in warm, oligotrophic waters (light blue).

Martino, Craig and Dustin point out that a large percentage of ocean shoreline is now modified by engineering, with associated impacts on primary production. Burgeoning coastal human populations are expected to increase demands on fisheries in the future and food web productivity is already forecasted to decrease, due to the effects of climate change. Understanding the impacts of marine urbanisation on food webs is becoming increasingly important so that design of artificial structures minimises impacts on food webs and remediation efforts can be undertaken if necessary.

This research is published in Frontiers in Ecology and the Environment.

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.

Overall benefits of MPAs when we re-calculate total reproduction accounting for non-linear relationships between length and mass and mass and reproduction. Pink 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.

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. Left: the benefit of MPAs for average fish reproduction driven by differences in mean size. Right: the benefits of MPAs are enhanced because of the greater ‘inequality’ in the MPAs where fish sizes are larger and more variable..

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 research is published in the journal Frontiers in Ecology and the Environment.

How well do we understand the way body size affects populations?

We have all heard the saying “live fast, die young” but it doesn’t only apply to film stars; smaller life forms also abide by this rule. Microscopic phytoplankton cells can double in numbers every few days, while the much larger elephant lives almost 100 years and reproduces slowly. This relationship between body mass and the ‘pace of life’ is well known. But the underlying mechanisms are far from resolved.

A number of years ago, scientists proposed a theory to link the ‘pace of life’ of individuals to the ecology of populations, communities, and ecosystems. The Metabolic Theory of Ecology predicts how energy use (metabolism) is affected by body size and how growth rate, development time and death rates change with energy use. These changes in individual rates will, in turn, affect rates of change in populations.

Metabolic Theory is very appealing because it explains many patterns we see in nature and is based on a fundamental rate which applies to all levels of organisation. But it is difficult to test. Detecting differences in energy use accurately requires having consistent differences in body sizes among organisms, while controlling for other variables (e.g. age, nutrition, health). This usually means comparing across species, which differ in more ways than just size.

The artificially evolved phytoplankton were almost 400 generations old when this work was done. The graph shows the considerable differences in size between small and large algae which allowed Martino and Dustin to ask their questions about body size, metabolism and populations within a species.

Few tests of these predictions have been able to control for these variables but recently Martino Malerba and Dustin Marshall were able to do this and they found that the body size-metabolism relationship did not predict population change as expected.

Martino and Dustin were in the enviable position of having access to artificially-evolved large and small phytoplankton cells of the same species that differed in size enough for them to ask “what happens to the population of a species if the average body size of individuals change?” They could see how body size affected energy use, growth rates, density and biomass.

It turns out that the story was far more complex than expected. The effect of body size on how organisms use energy and grow was very strong but also varied during the course of evolution.

So why didn’t body size explain trends in growth and energy use among size-evolved organisms? The answer may lie with previous work from the Centre for Geometric Biology. Martino and his colleagues found that large-evolved plankton cells optimized their photosynthetic pigments and produced more energy overall than smaller cells. This suggests larger cells have greater access to resources than smaller cells and so the way in which body size and metabolic rate influence the demography of a species is not as predictable as we once thought.

Instead of the classical view, where body size determines the rate at which organisms use energy, which then determines demographics, Martino and Dustin suggest that body size can affect metabolism and populations at the same time.

IIf these laboratory cultures are representative of natural populations, we would predict that current trends of reduced body size (from global warming) could lead to lower rates of population increase, biomass productivity and maximum biomass. This is the opposite of what current theory would predict. This is particularly important when we consider the role of phytoplankton in fixing carbon and supporting food chains.

This research was published in Ecology Letters.

How does size, fragmentation and food affect metabolic rates in a bryozoan?

We know that metabolic rate (a measure of energy use) tends to vary among individuals of different sizes and also with food availability. Lukas Schuster has been working with his PhD supervisors Craig White and Dustin Marshall to find out how metabolic rate changes with size in the colonial marine invertebrate Bugula neritina. They are also interested in how (or if) manipulating an organism’s size affects metabolic rate in individuals that were either starved or fed.

Lukas and his supervisors chose to work with Bugula because it is a colonial organism. These types of animals can be used for testing metabolic theories because the size of the colonies can be changed by removing fragments.

Lukas measured metabolic rate by measuring oxygen consumption of intact and size-manipulated colonies of Bugula that had been fed or starved as well as colonies that he had grown up in the field so he knew how old they were.

When Lukas measured metabolic rates for individuals of known age he found that rates increased proportionally with size across the different ages, that is, metabolic rate scaled isometrically with size when looking at individuals that ranged in age / developmental stage.  In contrast, when he looked at metabolic rates for a specific age or developmental stage he found that rates didn’t scale proportionally with size but, instead, had allometric scaling as has been found in previous studies.

Lukas and his supervisors point out that it is important to be aware of these differences. Measuring metabolic rates of field-collected specimens of unknown age may result in isometric scaling of metabolic rate with size. Conversely, measurements of specimens at the same developmental stage is likely to result in allometric scaling where larger individuals have proportionally lower metabolic rates compared to smaller individuals.

To the team’s surprise, they also found that when they measured metabolic rate in size-manipulated Bugula that has been collected from the field, metabolic rate reverted to allometric scaling. Manipulating size in Bugula may lead to a leaking of nutrients through the pores between the zooids that make up the colony and this may be driving the change in the relationship of metabolic rates with size.

Bugula responded to food deprivation by reducing its metabolic rate, and conversely responded to feeding by increasing its metabolic rate, which was consistent with what other researchers have found in other species. But, in comparison to other species, the rate at which Bugula increased its metabolic rate following feeding, was rather low. This may also relate to the fact that Bugula is a colonial species but as there are very few studies investigating the way metabolic rate responds to feeding in colonial organisms, it is hard to know for sure.

Clearly, the relationship between size and metabolic rates in Bugula is complicated and may relate, in part, to the fact that Bugula is a colonial organism. But to fully understand the effects of size manipulation on metabolic rates and biological processes within Bugula colonies, further studies will be needed.

This research is published in the journal Invertebrate Biology.