Are there any advantages to being smaller in higher temperatures?

Biologists have been familiar with a pattern of smaller body sizes with increasing temperatures for a long time, in fact, so familiar that Bergmann dubbed a “Temperature-Size Rule” in 1847.

Like many things to do with size, it is difficult to separate the effects of temperature on size from other traits that co-vary with size; metabolism for example. It may be that higher temperatures cause the evolution of faster metabolic rates and metabolic rate is genetically correlated with size. So that it is, in fact, metabolic rate that is the target of selection, not size.

Martino Malerba and Dustin Marshall were again able to take advantage of the evolved large and small algal cells to see if they could unambiguously assign any effects of temperature on size, to size alone. They wanted to find out if (and how) temperature affected fitness for different sized organisms.

To do this they used algal cells that had experienced 290 generations of artificial selection and where large selected cells were 13 times bigger than small selected cells. They then exposed these different lines (including the control lines) to three temperatures 18 °C, 22 °C and 26 °C and measured cell size, population density and cell production rates after three and six days.

They found that the smaller cells did better at higher temperatures; that is, the fitness proxies of cell production rate and population densities were both greater for small cells at higher temperatures. This means that Martino and Dustin have shown that size on its own can affect performance across different temperatures.

They then wanted to know why are cells smaller at higher temperatures; what is the advantage? It has long been thought that smaller cells do better in warmer temperatures because they have a greater surface-area to volume ratio. This would make them better able to take up resources such as nutrients, CO2 and light at the same time as increasing temperatures increase a cell’s demand for resources through increased enzyme activity and protein synthesis.

If this was the case, Martino and Dustin expected the large and small cells to show differences in performance at higher temperatures when resources were abundant (days 0 to 3) compared to when resources were depleted (days 3 to 6). But they found no difference in the fitness of large and small cells that related to resources suggesting that advantages of smaller cells at higher temperatures was not related to a greater surface-area to volume ratio.

Instead they measured the concentrations of reactive oxygen species in their selected lines of large and small cells. Reactive oxygen species are known to increase oxidative stress, damage DNA and so reduce the performance of a cell and also accumulate at higher temperatures. Martino found that the larger cells had almost five times more reactive oxygen species than smaller cells. And the larger cells had relatively smaller nuclei, meaning that there was twice the reactive oxygen species loading around the nuclei in large selected cells.

Martino and Dustin think that it is likely that small cells do better at higher temperatures, not because they are able to access more resources per unit volume, but because they are less prone to toxicity from reactive oxygen species.

This research was published in the journal Evolution.

Effects of two years of artificial size-selection (290 generations) on the cell volume of a phytoplankton species (Dunaliella tertiolecta).
Fitness increased with temperature (positive slope) in small-selected algae and decreased with temperature (negative slope) in large-selected algae. This finding confirms that reducing the size of a species automatically provides a fitness benefit at warmer temperatures.

Water temperatures and viscosity will both change with ocean warming but how will they affect male fertility in the tubeworm Galeolaria?

Global warming will increase ocean temperatures at the same time as it reduces seawater viscosity and Evatt Chirgwin wanted to know how this combination of physiological and physical change would affect male fertility in a small tubeworm. He found that both these factors independently reduced male fertility, and together altered selection pressures on sperm morphology.

Most marine species release gametes into the water column and successful fertilisation depends on a sperm locating and fusing with an egg. This high-risk strategy is in stark contrast with many terrestrial species where sperm and eggs interact in the controlled environment of a female reproductive tract, making marine species more vulnerable to global warming.

Projected ocean temperature increases are expected to reduce male fertility because exposure to temperatures outside the usual range can disrupt physiological processes and cell function. But the viscosity or ‘thickness’ of the seawater will also change with increasing temperatures, and Evatt was interested in understanding how the fact that sperm are able to move more easily through the water would affect male fertility.

Because these two things tend to change together, up until now no one has considered how decreases in viscosity at higher temperatures might alter fertility as well as selection pressure on sperm structure. Sperm with larger heads have increased ‘drag’ while a long tail can increase swimming speeds – these might not matter so much when seawater is easier to pass through.

So how do temperature and viscosity affect male fertility and the selection forces acting on the size and shape of sperm? Evatt and his supervisors (Keyne Monro and Dustin Marshall) measured fertilisation success at three temperatures and used a hydrophilic polymer that allows warmer water to be adjusted to the same viscosity as cooler water (but not the other way around).

Evatt measured head size, midpiece size and tail length in the sperm of 157 males that had access to eggs from a variety of females in five different fertilisation environments.

Evatt manipulated both temperature and viscosity to give five fertilisation environments for the 157 males that he had measured head size, midpiece size and tail length in the sperm. Sperm from each male added to eggs from a number of different females in each of the five environments and fertilisation success recorded.

The team found that the isolated effects of temperature and viscosity each caused fertility to decline by around 5% from current to moderate warming and by another 5% from moderate to extreme warming. But temperature and viscosity acted together to alter selection on sperm morphology. The ‘midpiece’ that houses the mitochondria, was a target for selection at the projected, warmer environments. A shorter midpiece was favoured in moderate warming environments, while a wider midpiece was favoured at the more extreme, longer-term projections of warming.

Sperm midpiece size was a target of selection with both temperature and viscosity acting in combination. Narrower midpieces are favoured by current conditions, shorter midpieces are favoured by projected warming environments and more extreme or longer term warming favoured wider midpieces.

Evatt and his supervisors think that since the midpiece contain the mitochondria that provide energy, it is probable that changes in temperature and viscosity will change the energy requirements of sperm during the location and fertilisation of eggs.

For the first time, the team show how projected changes in water temperature and viscosity may impact the fertility of marine populations and expose sperm to novel evolutionary pressures that may drive them to adapt in response.

This research was published in the journal Functional Ecology.

Size and reproduction: compiling a database

In 2018, 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 past 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?

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 credits: Alligator – skeeze via Pixabay. Centipede – Marshal Hedin via Wikimedia Commons.

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’.

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. They will also be able to use the ‘duplicate’ database look at how relationships between size and reproductive output vary through space and time.

Research fellow position: ecologist / evolutionary biologist

  • Level A, research-only academic
  • $68,040 – $92,343 pa (plus 9.5% employer superannuation)
  • Full-time, starting early 2020
  • One year, fixed term with the possibility of extension to a second year
  • Monash University Clayton campus

Professor Dustin Marshall is seeking an experienced ecologist / evolutionary biologist, who specialises in microalgal biology with a strong empirical background, to explore the ways in which size affects the structure and function of marine phytoplankton. This position will be with the Centre for Geometric Biology within the School of Biological Sciences at Monash University.

As the successful candidate, you will be expected to maintain the Centre’s evolved lines of the microalgae Dunaliella and use these evolved microalgae to undertake experiments that test ecological and evolutionary theories. You will also have a strong quantitative background and have a demonstrated track record in producing high-quality publications.

Key selection criteria

  1. A doctoral qualification in empirical ecology / evolutionary biology using microalgae as a model species.
  2. Demonstrated analytical and manuscript preparation skills; including an excellent track record of refereed research publications in high impact journals.
  3. Demonstrated experience in empirical research using cutting-edge quantitative approaches.
  4. Strong leadership, organisational and project management skills.
  5. Ability to work collaboratively with others

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

For more information, or to apply, refer to the Monash University website

Everybody loves good neighbours, but what makes a good neighbour?

Animals and plants compete for resources and traditionally we have held the view that competition drives interactions between species relying on the same resources. But Hayley Cameron and Dustin Marshall have shown it is not all about competition. Previously, we described Hayley’s PhD work where she demonstrated that large individuals did not outcompete their smaller neighbours, but instead facilitated their access to resources. But is that still true when the neighbours are a different species?

Hayley and Dustin have now looked at this in more detail. Collaborating with Tim Coulson from the University of Oxford, they varied the size and number of one species to see if it would affect the survival, growth and reproduction of a second species. They wanted to know how populations are affected when the size and numbers of neighbours vary.

The team used two common, filter-feeding, marine invertebrates shown to compete for food, space and oxygen. Watersipora is an ‘encrusting’ species that grows across surfaces, often growing over other organisms. Bugula has a ‘tree-like’ growth form and can efficiently harvest food and oxygen.

Both species are colonial invertebrates, made up of individual zooids. Watersipora and Bugula colonies were trimmed, creating a range of sizes and then a single Watersipora colony was placed on a small PVC plate and surrounded by different numbers of Bugula colonies. In total, they had 240 small plates hanging in Port Phillip Bay for 8 weeks.

Hayley, Tim and Dustin were interested in the consequences for populations when species of different sizes interact. So, they used a particular type of mathematical model called an Integral Projection Model. They entered data on survival, growth and reproduction of Watersipora for each size and number of Bugula neighbours. The model calculated the population growth rate for Watersipora with different neighbour combinations.

They found population growth of Watersipora was greatest when there were many, small Bugula neighbours. Large Bugula in the neighbourhood meant slow population growth of Watersipora; the species’ competed for resources and the more, large Bugulathere were, the greater the competition.

We know Bugula disrupts water flow and affects the delivery of food and oxygen to Watersipora. It seems, many small Buguladisrupt water flow and more food and oxygen reach the Watersipora. But while large Bugula also slow water flow, they consume more resources leaving a net negative effect on Watersipora.

So, both size and density played a part in determining whether a neighbour facilitated or competed with a target species. This means different population size structures will yield different outcomes in terms of species interactions. Hayley, Tim and Dustin emphasise that size should be included in studies of competition as any conclusions about how two species interact will depend on the size and density of the proposed competitor.

What is particularly exciting about these results is that the team may have uncovered an alternative pathway through which species using the same resources can co-exist. If body size mediates a switch between facilitation and competition then co-existence is more possible than previously simple experiments would imply.

This research was published in the journal Ecology Letters.

Powering ocean giants: the energetics of shark and ray megafauna

Authors: Christopher L Lawson, Lewis G Halsey, Graeme C Hays, Christine L Dudgeon, Nicholas L Payne, Michael B Bennett, Craig R White, and Anthony J Richardson

Published in: Trends in Ecology & Evolution

Highlights

Energetics studies have illuminated how animals partition energy among essential life processes and survive in extreme environments or with unusual lifestyles. There are few bioenergetics measurements for elasmobranch megafauna; the heaviest elasmobranch for which metabolic rate has been measured is only 47.7 kg, despite many weighing >1000 kg.

Bioenergetics models of elasmobranch megafauna would answer fundamental ecological questions surrounding this important and vulnerable group, and enable an understanding of how they may respond to changing environmental conditions, such as ocean warming and deoxygenation.

Larger chambers and swim-tunnels have allowed measurements of the metabolism of incrementally larger sharks and rays, but laboratory systems are unlikely to be suitable for the largest species.

Novel uses of biologging and collaboration with commercial aquaria may enable energetics of the largest sharks and rays to be measured.

Innovative use of technology and models derived from disparate disciplines, from physics to artificial intelligence, can improve our understanding of energy use in this group.

Shark and ray megafauna have crucial roles as top predators in many marine ecosystems, but are currently among the most threatened vertebrates and, based on historical extinctions, may be highly susceptible to future environmental perturbations. However, our understanding of their energetics lags behind that of other taxa. Such knowledge is required to answer important ecological questions and predict their responses to ocean warming, which may be limited by expanding ocean deoxygenation and declining prey availability. To develop bioenergetics models for shark and ray megafauna, incremental improvements in respirometry systems are useful but unlikely to accommodate the largest species. Advances in biologging tools and modelling could help answer the most pressing ecological questions about these iconic species.

Lawson CL, Halsey LG, Hays GC, Dudgeon CL, Payne NL, Bennett MB, White CR, Richardson AJ (2019) Powering ocean giants: the energetics of shark and ray megafauna. Trends in Ecology & Evolution PDF DOI

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).