Director’s message

The Centre for Geometric Biology entered its third 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.

Prof Dustin Marshall, Director
Prof Craig White, Deputy Director

ANNUAL REPORT 2017

Understanding variation in metabolic rate

Authors: Amanda K Pettersen, Dustin J Marshall, and Craig R White

Published in: The Journal of Experimental Biology

Abstract

Metabolic rate reflects an organism’s capacity for growth, maintenance and reproduction, and is likely to be a target of selection. Physiologists have long sought to understand the causes and consequences of within-individual to among-species variation in metabolic rates – how metabolic rates relate to performance and how they should evolve.

Traditionally, this has been viewed from a mechanistic perspective, relying primarily on hypothesis-driven approaches. A more agnostic, but ultimately more powerful tool for understanding the dynamics of phenotypic variation is through use of the breeder’s equation, because variation in metabolic rate is likely to be a consequence of underlying microevolutionary processes.

Here we show that metabolic rates are often significantly heritable, and are therefore free to evolve under selection. We note, however, that ‘metabolic rate’ is not a single trait: in addition to the obvious differences between metabolic levels (e.g. basal, resting, free-living, maximal), metabolic rate changes through ontogeny and in response to a range of extrinsic factors, and is therefore subject to multivariate constraint and selection.

We emphasize three key advantages of studying metabolic rate within a quantitative genetics framework: its formalism, and its predictive and comparative power.

We make several recommendations when applying a quantitative genetics framework: (i) measuring selection based on actual fitness, rather than proxies for fitness; (ii) considering the genetic covariances between metabolic rates throughout ontogeny; and (iii) estimating genetic covariances between metabolic rates and other traits.

A quantitative genetics framework provides the means for quantifying the evolutionary potential of metabolic rate and why variance in metabolic rates within populations might be maintained.

Pettersen AK, Marshall DJ, White CR (2018) Understanding variation in metabolic rate, The Journal of Experimental Biology, PDF DOI

Ocean sunfish as indicators for the ‘rise of slime’

Authors: David Grémillet, Craig R White, Matthieu Authier, Ghislain Dorémus, Vincent Ridoux, and Emeline Pettex

Published in: Current Biology

Summary

Overfishing and ocean warming are drastically altering the community composition and size structure of marine ecosystems, eliminating large bodied species. Against a backdrop of such environmental change, the heaviest of all bony fish, the ocean sunfish (Mola mola), seems an improbable survivor. Indeed this indolent giant is killed globally as bycatch, and is listed as ‘Vulnerable’.

Sunfish are so named because they engage in extensive sunbathing at the water surface making them far easier to monitor than jellyfish. Image credit: Mike Baird via Flickr.

We undertook the most extensive aerial surveys of sunfish ever conducted and found surprisingly high abundances off the Atlantic and Mediterranean coasts of Western Europe. With up to 475 individuals per 100 square kilometres, these figures are one order of magnitude higher than abundance estimates for other areas. Using bioenergetic modelling, we estimate that each sunfish requires 71 kilograms per day of jellyfish, a biomass intake more than an order of magnitude greater than predicted for a similarly sized teleost. Scaled up to the population level, this equates to a remarkable 20,774 tonnes per day of predated jellyfish across our study area in summer.

Sunfish abundance may be facilitated by overfishing and ocean warming, which together cause reduced predation of sunfish by sharks and elevated jellyfish biomass. Our combined survey and bioenergetic data provide the first-ever estimate of spatialized ocean sunfish daily food requirements, and stress the importance of this species as a global indicator for the ‘rise of slime’.

This hypothesis posits that, in an overfished world ocean exposed to global warming, gelatinous zooplankton should flourish, to the detriment of other mesotrophic species such as small pelagic fish, causing irreversible trophic cascades as well as a series of other environmental and economic issues.

Grémillet D, White CR, Authier M, Dorémus G, Ridoux V, Pettex E (2017) Ocean sunfish as indicators for the ‘rise of slime’, Current Biology, PDF DOI 

Atmospheric trace gases support primary production in Antarctic desert surface soil

Authors: Mukan Ji, Chris Greening, Inka Vanwonterghem, Carlo R Carere, Sean K Bay, Jason A Steen, Kate Montgomery, Thomas Lines, John Beardall, Josie van Dorst, Ian Snape, Matthew B Stott, Philip Hugenholtz and Belinda C Ferrari

Published in: Nature

Abstract

Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities. Given that phototroph abundance varies across these Antarctic soils, an enduring question is what supports life in those communities with low photosynthetic capacity.

Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities.

We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation.

Soil microcosms aerobically scavenged atmospheric H2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO2 fixation.

We propose that atmospheric H2, CO2 and CO provide dependable sources of energy and carbon to support these communities, which suggests that atmospheric energy sources can provide an alternative basis for ecosystem function to solar or geological energy sources.

Although more extensive sampling is required to verify whether this process is widespread in terrestrial Antarctica and other oligotrophic habitats, our results provide new understanding of the minimal nutritional requirements for life and open the possibility that atmospheric gases support life on other planets.

Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, Montgomery K, Lines T, Beardall J, van Dorst J, Snape I, Stott MB, Hugenholtz P, Ferrari BC (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil, Nature, PDF DOI 

Metabolic theory: how does the cost of development scale allometrically with offspring size?

One of the most fundamental patterns studied in life-history theory is how offspring size links to performance of an individual. Within species, larger offspring generally have higher survival, reproductive output and growth, and lower risk of predation and starvation. One key question that remains is why larger offspring outperform smaller offspring.

The Centre’s Amanda Pettersen and colleagues Craig White, Robert Bryson-Richardson and Dustin Marshall explored one potentially widespread mechanism: how the costs of development scale with offspring size, using metabolic theory. Metabolic theory proposes that there is an allometric relationship between energy use (metabolic rate) and body size, where on a log-log scale, the slope of this relationship is less than one.

Amanda and colleagues sought to explore whether the same pattern (i.e allometric scaling) occurs with offspring size, in order to understand how size affects the relative use of energy reserves throughout a critical life period. They measured embryo mass and metabolic rate throughout development, from fertilisation to hatching, in the freshwater fish, Danio rerio.

3-hour old embryos of the tropical freshwater zebrafish, Danio rerio.

The team found an allometric relationship between embryo mass and metabolic rate – while larger offspring use absolutely more energy, they also use relatively less energy to reach the end of development, than smaller offspring. Larger offspring use proportionally less of their supplied energy to reach the end of development than smaller offspring. These findings are supported by the observation that hatchlings from larger embryos are both disproportionately heavier and retain relatively more of their initial energy reserves than smaller embryos. These findings mean that the same allometric scaling relationships that are found for adult body size also apply for offspring size. But they also may explain a fundamental pattern in life-history theory: allometric scaling with offspring size may serve as a widely applicable explanation for why larger offspring often perform better than smaller offspring.

This research in published in the journal Functional Ecology.

Eco-energetic consequences of evolutionary shifts in body size

Authors: Martino E Malerba, Craig R White, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Size imposes physiological and ecological constraints upon all organisms. Theory abounds on how energy flux covaries with body size, yet causal links are often elusive.

As a more direct way to assess the role of size, we used artificial selection to evolve the phytoplankton species Dunaliella tertiolecta towards smaller and larger body sizes.

Within 100 generations (c. 1 year), we generated a fourfold difference in cell volume among selected lineages. Large-selected populations produced four times the energy than small-selected populations of equivalent total biovolume, but at the cost of much higher volume-specific respiration. These differences in energy utilisation between large (more productive) and small (more energy-efficient) individuals were used to successfully predict ecological performance (r and K) across novel resource regimes.

We show that body size determines the performance of a species by mediating its net energy flux, with worrying implications for current trends in size reduction and for global carbon cycles.

Malerba ME, White CR, Marshall DJ (2017) Eco-energetic consequences of evolutionary shifts in body size, Ecology Letters, PDF DOI 

Does the cost of development scale allometrically with offspring size?

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson-Richardson, and Dustin J Marshall

Published in: Functional Ecology

Summary

Within many species, larger offspring have higher fitness. While the presence of an offspring size-fitness relationship is canonical in life-history theory, the mechanisms that determine why this relationship exists are unclear.

Linking metabolic theory to life-history theory could provide a general explanation for why larger offspring often perform better than smaller offspring. In many species, energy reserves at the completion of development drive differences in offspring fitness. Development is costly so any factor that decreases energy expenditure during development should result in higher energy reserves and thus subsequently offspring fitness.

Metabolic theory predicts that larger offspring should have relatively lower metabolic rates and thus emerge with a higher level of energy reserves (assuming developmental times are constant). The increased efficiency of development in larger offspring may therefore be an underlying driver of the relationship between offspring size and offspring fitness, but this has not been tested within species.

To determine how the costs of development scale with offspring size, we measured energy expenditure throughout development in the model organism Danio rerio across a range of natural offspring sizes. We also measured how offspring size affects the length of the developmental period. We then examined how hatchling size and condition scale with offspring size.

We find that larger offspring have lower mass-specific metabolic rates during development, but develop at the same rate as smaller offspring. Larger offspring also hatch relatively heavier and in better condition than smaller offspring. That the relative costs of development decrease with offspring size may provide a widely applicable explanation for why larger offspring often perform better than smaller offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2017) Does the cost of development scale allometrically with offspring size?, Functional Ecology, PDF DOI