The Conversation: From crocodiles to krill, a warming world raises the ‘costs’ paid by developing embryos

By Dustin Marshall

This article is republished from The Conversation under a Creative Commons licence.

Apart from mammals and birds, most animals develop as eggs exposed to the vagaries of the outside world. This development is energetically “costly”. Going from a tiny egg to a fully functioning organism can deplete up to 60% of the energy reserves provided by a parent.

In cold-blooded animals such as marine invertebrates (including sea stars and corals), fish and reptiles, and even insects, embryonic development is very sensitive to changes in the temperature of the environment.

Thus, in a warming world, many cold-blooded species face a new challenge: developing successfully despite rising temperatures.

For our research, published today in Nature Ecology and Evolution, we mined existing literature for data on how temperature impacts the metabolic and development rates of 71 different species, ranging from tropical crocodiles to Antarctic krill.

We found over time, species tend to fine-tune their physiology so that the temperature of the place they inhabit is the temperature needed to minimise the “costs” of their embryonic development.

Temperature increases associated with global warming could substantially impact many of these species.

The perfect weather to grow an embryo

The energy costs of embryonic development are determined by two key rates. The “metabolic” rate refers to the rate at which energy is used by the embryo, and the “development” rate determines how long it takes the embryo to fully develop, and become an independent organism.

Both of these rates are heavily impacted by environmental temperature. Any change in temperature affecting them is therefore costly to an embryo’s development.

Generally, a 10°C increase in temperature will cause an embryo’s development and metabolic rate to more than triple.

This photo shows a developing sea urchin, from egg (top left) to larva, to a metamorphosed (matured into adult form) individual.

These effects partially cancel each other out. Higher temperatures increase the rate at which energy is used (metabolic), but shorten the developmental time.

But do they balance out effectively?

What are the costs?

For any species, there is one temperature that achieves the perfect energetic balance between relatively rapid development and low metabolism. This optimal temperature, also called the “Goldilocks” temperature, is neither too hot, nor too cold.

When the temperature is too cold for a certain species, development takes a long time. When it’s too hot, development time decreases while the metabolic rate continues to rise. An imbalance on either side can negatively impact a natural population’s resilience and ability to replenish.

As an embryo’s developmental costs increase past the optimum, mothers must invest more resources into each offspring to offset these costs.

When offspring become more costly to make, mothers make fewer, larger offspring. These offspring start life with fewer energy reserves, reducing their chances of successfully reproducing as adults themselves.

Thus, when it comes to embryonic development, higher-than ideal temperatures pack a nasty punch for natural populations.

Since the temperature dependencies of metabolic rate and development rate are fairly similar, the slight differences between them had gone unnoticed until recently.

Embryos at risk

For each species in our study, we found a narrow band of temperatures that minimised developmental cost. Temperatures that were too high or too low caused massive blow-outs in the energy budget of developing embryos.

This means temperature increases associated with global warming are likely to have bigger impacts than previously predicted.

Predictions of how future temperature changes will affect organisms are often based on estimates of how temperature affects embryo survival. These measures suggest small temperature increases (1°C-2°C) do not reduce embryo survival by much.

But our study found the developmental costs are about twice as high, and we had underestimated the impacts of subtle temperature changes on embryo development.

In the warming animal kingdom, there are winners and losers

Some good news is our research suggests not all species are facing rising costs with rising temperatures, at least initially.

We’ve created a mathematical framework called the Developmental Cost Theory, which predicts some species will actually experience slightly lower developmental costs with minor increases in temperature.

In particular, aquatic species (fish and invertebrates) in cool temperate waters seem likely to experience lower costs in the near future. In contrast, certain tropical aquatic species (including coral reef organisms) are already experiencing temperatures that exceed their optimum. This is likely to get worse.

It’s important to note that for all species, increasing environmental temperature will eventually come with costs.

Even if a slight temperature increase reduces costs for one species, too much of an increase will still have a negative impact. This is true for all the organisms we studied.

A key question now is: how quickly can species evolve to adapt to our warming climate?The Conversation

Developmental cost theory predicts thermal environment and vulnerability to global warming

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

Published in: Nature Ecology & Evolution

Abstract

Metazoans must develop from zygotes to feeding organisms. In doing so, developing offspring consume up to 60% of the energy provided by their parent.

The cost of development depends on two rates: metabolic rate, which determines the rate that energy is used; and developmental rate, which determines the length of the developmental period. Both development and metabolism are highly temperature-dependent such that developmental costs should be sensitive to the local thermal environment.

Here, we develop, parameterize and test developmental cost theory, a physiologically explicit theory that reveals that ectotherms have narrow thermal windows in which developmental costs are minimized (Topt).

Our developmental cost theory-derived estimates of Topt predict the natural thermal environment of 71 species across seven phyla remarkably well (R2⁓0.83).

Developmental cost theory predicts that costs of development are much more sensitive to small changes in temperature than classic measures such as survival. Warming-driven changes to developmental costs are predicted to strongly affect population replenishment and developmental cost theory provides a mechanistic foundation for determining which species are most at risk. Developmental cost theory predicts that tropical aquatic species and most non-nesting terrestrial species are likely to incur the greatest increase in developmental costs from future warming.

Marshall DJ, Pettersen AK, Bode M, White CR (2020) Developmental cost theory predicts thermal environment and vulnerability to global warming. Nature Ecology & Evolution DOI EPDF

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.

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.

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.