Annual Report 2017

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.

 

 

Director’s message

The Centre for Geometric Biology entered its 3rd year in 2017.  It has been an extremely busy year with many research highlights.  The different research groups are working with a variety of organisms and approaches to explore a wide range of specific questions about organismal growth.  There has been a palpable feeling of excitement as the different research streams and collaborations are starting to come together under the unifying theme of energy acquisition and use.

Success in the realms of external funding and publications in high ranking journals has been excellent in 2017 and this applies to all career levels from PhD students to early career researchers and above.

A meeting with board members and the Monash University internal review process has provided ample opportunity to reflect on our progress and identify where we want to be headed.  A priority target is to improve the theoretical underpinning of our work.  Successful visits followed on from theoretical ecologist Professor Andre de Roos in 2016 (University of Amsterdam), with visits from mathematical modeler Professor Tim Coulson (University of Oxford) and theoretician Professor Troy Day (Queens University, Ontario) in 2017.  These visits have all resulted in ongoing collaborations and I think we have all found them highly motivating.

Finally, we would like to thank the board members and the internal review team for their ongoing interest and support of our research and of course congratulate all the members of the Centre for Geometric Biology for their many successes in 2017.

Director, Dustin Marshall and Deputy Director, Craig White.


Some research highlights from 2017

An experimental demonstration of the effect of competition on energy budgets

How much an individual organism can grow depends on both the amount of energy acquired (from food consumption) and the energy expended on respiration (metabolic rate).  Increasing population densities can affect the availability of energy by increasing competition for resources (such as food) which can, in turn, affect the rates at which individuals acquire and expend energy.

Post-doctoral fellow, Giulia Ghedini and colleagues Craig White and Dustin Marshall are interested in whether feeding rates and metabolic rates change in the same way when population densities increase. They wanted to explore why individuals typically reach smaller sizes in denser populations while knowing that growth ultimately depends on how rates of energy intake change relative to rates of energy expenditure.

The research team considered 4 possible scenarios where the rates of feeding and metabolism varied and which would have different outcomes in terms of the energy available for growth (see figure).  Few studies have considered both these rates at the same time and so the ways in which both intake (feeding) and expenditure (metabolism) are affected by density remains unclear making it difficult to predict which scenario would apply.

The research team considered four possible scenarios where the rates of feeding and metabolism varied and which would have different outcomes in terms of the energy available for growth.

Giulia and colleagues used the colonial bryozoan Bugula neritina as a study organism and experimentally created populations of different densities by settling increasing numbers of larvae on experimental plates. After metamorphosis these larvae developed into adult colonies that were grown in the field at the different population densities ranging from 1 to 30 individual colonies per plate.

The different populations of Bugula were supplied with equal amounts of food (a single celled alga) and feeding rates were calculated after 3 hours.  Metabolic rates were calculated by measuring changes in % oxygen over the same period of time (3 hours) and the ‘scope for growth’ of each individual colony was calculated by subtracting energy expenditure (metabolism) from energy intake (feeding).

Giulia and her colleagues found that while both feeding rates and metabolic rates decreased with increasing population densities, energy gains from food intake decreased faster than the energy expended on metabolism, reducing the amount of energy available for growth (scenario 3 on figure).  This explains why individual growth and reproductive output decrease in denser populations.

What is more, the researchers have also demonstrated that the difference between energy intake and expenditure at the individual colony level could predict the average body size that colonies reached in populations of varying densities.

 

Evolving smaller body sizes improve the ability to persist when resources are limited, but at a cost.

We know that the growth and reproduction of an organism are dependent on both energy acquisition and energy use – net energy flux –  but few studies look at both these simultaneously.  Recent reductions in body size across a range of taxa worldwide, has focused attention on increasing our understanding about the role size plays in determining net energy flux.

Martino Malerba and co-authors Dustin Marshall and Craig White used a technique called artificial selection to genetically evolve small and large populations of a single celled marine alga Dunaliella tertriolecta that differed in size by 500%. They then assessed some physiological and ecological consequences of this size shift.

The research team found that under low energy conditions (ie low light intensities or short light durations) the smaller cells showed faster growth rates than control and larger cells and conversely under high energy conditions larger cells displayed faster growth rates. Surprisingly though, the smaller cells reached lower total biovolumes overall regardless of the light regime.

Other traits such as swimming speed and distance travelled showed the highest performance in the control cells; perhaps because they maintained an optimal ratio of cell size to length of swimming flagella.

These results emphasise that the costs and benefits of different cells sizes depend on the context.  In low resource environments smaller cells will have a greater ability to persist but will be less productive than larger cells, while in high resource environments larger cells will perform better.

This research, published in the highly regarded journal Ecology Letters, will inform the debate on how natural ecosystems will respond to human impacts. Open oceans are the most productive systems in the world and single celled algal species dominate this production. These results show that reductions in cell size as a result of human activities such as fishing and climate change can severely reduce this rate of carbon fixation by as much as 40%.

Scanning electron micrographs of artificially selected algae. “If the environment allows you to “acquire much”, be big! Otherwise, better to “desire little” and be little.

 

Mixing it up – methanotrophs use hydrogen as alternative energy source

Chris Greening, from the Centre for Geometric Biology, has been working with collaborators from GNS Science, University of Otago, Scion, and Montana State University, to provide evidence that aerobic methane-oxidising bacteria (methantrophs) are able to meet energy and biomass demands in variable environments, by using hydrogen as an alternative energy source.

Methanotrophs thrive in areas where methane (CH4) fluxes are high such as peat bogs, wetlands, rice paddies and geothermal habitats and have been considered specialist users of single carbon compounds such as methane.  But, these types of bacteria also exist within soil and marine systems where CH4 and oxygen (O2) concentrations fluctuate more widely.

This led Chris and colleagues to hypothesise that methanotrophs must be able to supplement metabolism of CH4 and O2 with other energy yielding strategies to support growth.

The research team conducted an interdisciplinary study to investigate the role of hydrogen (H2) as an important electron donor allowing organisms to meet carbon and energy demands in response to fluctuating CH4 and O2 availability.

Field studies demonstrated that bacteria in the phylum Verrumicrobia simultaneously oxidised CH4 and H2 in geothermally heated soils. What is more, laboratory studies confirmed that a representative of the Verrumicrobia depended on H2 consumption when CH4 and O2 were experimentally varied.

This evidence, coupled with genome surveys, led the researchers to conclude that H2 oxidation expands the ecological niche of methanotrophs, enabling them to meet energy and biomass demands in dynamic environments where O2 and CH4 concentrations are variable.

This finding has broad implications for future investigations into the ecology of methanotrophs – primary players in greenhouse-gas mitigation.

 

What happens in 60,000 generations of evolution?

Mike McDonald, working with colleagues from the United States, has found that long-term adaptation to a constant environment can be a more complex and dynamic process than is often assumed.

The team were able to observe this process directly by using frozen samples of E. coli from the ongoing experimental evolution study led by Richard Lenski, now in its 30th year. This is over 67,000 generations for each of the 12 replicate populations.

Previous studies have shown that the populations have not yet reached the expected ‘fitness peak’ despite tens of thousands of generations in the same environment.  While the competitive fitness of each generation continues to increase, the rate of improvement has slowed.

Through analysing genome sequences every 500 generations, Mike and the research team have been able to analyse when, and in what order, successful mutations occur, the dynamics by which they spread through a population and what other competing mutations have arisen.

Their data revealed a complex adaptive process with competition between lineages arising from different beneficial mutations important, but genetic drift and eco-evolutionary feedback also playing significant roles. In the latter instance the evolving E. coli change the environment they are growing in, which can, in turn, influence the evolutionary trajectories of the different populations.

The combination of such processes can help explain why the rate of molecular evolution in E. coli populations remains so high through 60,000 generations.

These results help us understand the complex population genetic processes that take place in the long term adaptation to a fixed environment and are in stark contrast to the ‘evolutionary desert’ expected near a fitness peak.

This figure shows the trajectories of different mutations in different populations. A mutation may become ‘fixed’ where 100% of all alleles have that mutation, others may reach substantial frequencies before becoming extinct. What was most striking however was when neither fixation or extinction occurred, with 9 of the 12 populations maintaining 2 or more stable “subpopulations”, within the culture. This indicates that one way the populations can continue to adapt for so long is by diversifying and evolving niche specific subpopulations.

Looking forward

Australian Research Council Discovery Projects to begin in 2018

Prof Dustin Marshall will be investigating how the paternal environment, that is, the environment that developing sperm experience, can influence reproductive and offspring success.  Dustin will use an externally fertilising marine invertebrate as his study organism which will allow him to manipulate the paternal environment without the confounding effect of the maternal environment.

Prof Craig White and Dr Lesley Alton will be tackling the fundamental biological question of why so few biological traits scale proportionally with body size. Craig and Lesley will use artificial selection to engineer animals where biological scaling laws are either ‘broken’ or enhanced. This means that they will create large animals with low metabolic rates and small animals with high metabolic rates and measure the consequences of this for fitness.

Dr Mike McDonald will be collaborating with Dr Kat Holt from the University of Melbourne to investigate the co-evolution of microbes in a long-term evolution experiment.  The bacteria E.coli and the baker’s yeast S. cerevisiae will be cultured independently or together in two different environments for 1000 generations. Mike and Kat will then measure individual growth rates, ecosystem performance, fitness, and sequence the whole genome. They will then look for signals of co-evolution between E.coli and yeast.

Dr. Chris Greening will be collaborating with Ass. Professor Perran Cook from the School of Chemistry and Ronnie Glud and Damien Callahan (University of Southern Denmark and Deakin University) to investigate the role that hydrogen plays in sandy sediments that are anoxic (depleted of oxygen). This project aims to quantify the respiratory pathways and the importance of hydrogen in the microbial ecology and biogeochemistry in the sandy sediments that dominate our coastline.

 


CGB quick view

Publications
50
scientific publications since CGB began in 2015
33
publications from the CGB in 2017
74.4%
publications in top 10% journals by Cite Score
30
citations received by publications 2015-2017

(Stats from SciVal 4 January 2018 based on 44 publications)

Communications
52
posts published on website in 2017
4,407
website visitors (more than double the number for 2016)
72
tweets in 2017

 

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

 

Events
1
symposium
6
workshops / visits hosted
4
workshops / visits hosted

Financial snapshot

  • Core funding received from Faculty of Science and School of Biological Science
  • 3 Future Fellowship
  • 3 ARC DECRAs
  • 1 Endeavour Fellowship
  • 2 ARC Discovery grants awarded in 2017
  • 4 more ARC Discovery grants to start in 2018

Full publications list

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 DR, Kulbicki M, Floeter SR, Friedlander AM & AP, A. (2016) Energetic and ecological constraints on population density of reef fishes. Proceedings of the Royal Society B: Biological Sciences, 283.

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.

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. (2016) Isolation drives taxonomic and functional nestedness in tropical reef fish faunas. Ecography.

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.

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., Jr. (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. The Isme Journal, 11, 2599.

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., Sgro, 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.

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.

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.

Ghedini, G. & Connell, S.D. (2016) Moving ocean acidification research beyond a simple science: Investigating ecological change and their stabilizers. Food Webs.

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

Gimenez, L., Torres, G., Pettersen, A., Burrows, M.T., Estevez, A. & Jenkins, S.R. (2017) Scale-dependent natural variation in larval nutritional reserves in a marine invertebrate: implications for recruitment and cross-ecosystem coupling. Marine Ecology Progress Series, 570, 141-155.

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.

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.

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.

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

Lange, R. & Marshall, D. (2017) Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Scientific Reports, 7, 6281.

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, 1-11.

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., 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.

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.

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, 3529.

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

Olito C, Marshall DJ & T, C. (2016) The evolution of reproductive phenology in broadcast spawners and the maintenance of sexually antagonistic polymorphism. The American Naturalist.

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., 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. (2016) Phylogenetic analysis of the allometry of metabolic rate and mitochondrial basal proton leak. Journal of Thermal Biology.

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.

Quistad, S.D., Grasis, J.A., Barr, J.J. & Rohwer, F.L. (2017) Viruses and the origin of microbiome selection and immunity. ISME J, 11, 835-840.

Svanfeldt K, Monro K & DJ, M. (2017) Field manipulations of resources mediate the transition from intraspecific competition to facilitation. Journal of Animal Ecology.

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

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.

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.