Authors: Mariana Álvarez-Noriega, Scott C Burgess, James E Byers, James M Pringle, John P Wares, and Dustin J Marshall
Published in:Nature Ecology & Evolution
The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed.
Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydro-dynamics also covary with latitude—these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale.
Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance.
We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations.
Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.
Álvarez-Noriega M, Burgess SC, Byers JE, Pringle JM, Wares JP, Marshall DJ (2020) Global biogeography of marine dispersal potential. Nature Ecology & Evolution PDFDOI
It is generally recognised that animals perform best at certain temperatures, so-called optimal temperatures. To understand how measures of performance, such as growth or running ability, will change with changing temperatures we need to understand the physiological processes limiting performance.
One compelling theory, known as the oxygen and capacity-limited thermal tolerance (OCLTT), suggests that a reduction in oxygen availability limits performance.
As temperature shifts away from optimal, the demand for oxygen in tissues is thought to outpace the rate of supply. This means a shift to anaerobic metabolism, a process far less efficient than aerobic metabolism, causing a reduction in performance.
Emily Lombardi, Candice Bywater and Craig White wanted to test the theory and used the speckled cockroach as their experimental animal because they are easy to breed and keep in the lab. Unlike other studies testing the OCLTT hypothesis, their interest was in the less extreme ends of the temperature range, which the OCLTT hypothesis specifically addresses.
First, Emily and her colleagues calculated the temperature that optimised growth by allowing juvenile cockroaches to develop for 35 days at 8 temperatures ranging between 10 and 36 °C. They also determined the temperatures (both above and below the optimal temperature) where growth was reduced by 32%. These 3 temperatures (optimal, lower and upper developmental temperatures) were then used in oxygen manipulation experiments.
Next, they ran an experiment including the three temperatures plus three oxygen concentrations; atmospheric (21%), hypoxic (10%) and hyperoxic (40%). Cockroaches were assigned to one of the 9 treatments and growth rate was measured repeatedly over 5 weeks. Running performance – time on a treadmill – was measured at the end of the 5 weeks at the three temperatures. Tracheal morphology was also quantified because, in some species, changes to the oxygen delivery system can alleviate the demand for increased oxygen supply.
If the OCLTT theory held, then the team expected to see a difference in performance at the different oxygen concentrations at each temperature. But, instead, they found increasing oxygen concentrations did not mitigate the effects of sub-optimal temperatures. There was also no evidence that tracheal morphology changed as a result of the developmental temperature or oxygen environment. The team concluded that oxygen supply was not the main determinant of temperature-related performance limitations for the speckled cockroach.
It seems, the OCLTT may not provide the unifying theory its proponents hoped, but instead, a species’ thermal tolerance is likely shaped by a range of factors.
We know that the rate at which organisms use energy (metabolic rate) varies substantially between individuals of the same species, even after accounting for size and temperature. What we are less sure about, is, why we see this variation.
When Amanda Pettersen and her colleagues thought about this question they considered it plausible that the competitive environments that individuals find themselves in might be important in determining whether a faster or slower metabolic rate is selected for. They wanted to find out whether variation in competition affects selection on metabolic rates and whether that could account for the variation in metabolic rate that persists more generally.
To test this idea Amanda used the model species Bugula neritina because it allowed the team to collect larvae in the lab, measure size and metabolic rate of larvae before assigning the larvae to one of three ‘competition’ treatments. Once the larval measurements were made, larvae were randomly assigned to either a no-competition environment, a competitive environment where they were put with other Bugula neritina (intraspecific competition) or, a competitive environment with an established mixed-species community (interspecific competition).
Individuals were then returned to the field and monitored weekly for survival, growth, age when first become reproductive and fecundity (total reproductive output).
The team already knew that higher metabolic rates are linked to faster growth, earlier onset of reproduction, and a shorter lifespan, while low metabolic rates are associated with a slow pace-of-life (slow growth, late onset of reproduction and long lifespan).
This experiment showed that individuals with higher metabolic rates were more likely to survive, more likely to reproduce and had greater numbers of ovicells at the start of reproduction, in the more intense, interspecific competition treatment. The team speculates that the individuals with higher metabolic rates grow more quickly enabling them to reach resources such as food and oxygen that are less available to smaller, slower growing organisms. There is a downside: these higher metabolic rate individuals also had a shorter lifespan.
The expectation amongst evolutionary biologists is that where there is strong selection pressure for a particular trait then the variation within that trait is reduced. So even accounting for the shorter lifespan, the overall increase in reproduction should mean that a higher metabolic rate is strongly selected for in competitive environments.
But the team also found that individuals with lower metabolic rates had a higher probability of living for longer in the absence of competition and would have continued to reproduce long after the individuals with a higher metabolic rate had died.
Bugula live on hard substrates and these areas commonly vary in their composition. Complex three-dimensional, highly diverse communities are interspersed with sparse populations of a few species and patches of bare areas. Individuals with lower metabolic rates that happen to arrive at a bare patch will have a long reproductive period and high overall fecundity. In contrast, individuals with a high metabolic rate that settle in amongst other species will be reproductive quickly and so successfully produce large numbers of offspring.
Because Bugula larvae are likely to find themselves in a variety of different competitive environments – even when they settle relatively close to each other – there is a strong evolutionary argument to explain the persistence of variation in metabolic rate, for Bugula at least.
Authors: Amanda K Pettersen, Matthew D Hall, Craig R White, and Dustin J Marshall
Published in:Evolution Letters
Metabolism is linked with the pace-of-life, co-varying with survival, growth, and reproduction. Metabolic rates should therefore be under strong selection and, if heritable, become less variable over time. Yet intraspecific variation in metabolic rates is ubiquitous, even after accounting for body mass and temperature.
Theory predicts variable selection maintains trait variation, but field estimates of how selection on metabolism varies are rare.
We use a model marine invertebrate to estimate selection on metabolic rates in the wild under different competitive environments.
Fitness landscapes varied among environments separated by a few centimetres: interspecific competition selected for higher metabolism, and a faster pace‐of‐life, relative to competition‐free environments.
Populations experience a mosaic of competitive regimes; we find metabolism mediates a competition-colonization trade-off across these regimes. Although high metabolic phenotypes possess greater competitive ability, in the absence of competitors, low metabolic phenotypes are better colonizers.
Spatial heterogeneity and the variable selection on metabolic rates that it generates is likely to maintain variation in metabolic rate, despite strong selection in any single environment.
Pettersen AK, Hall MD, White CR, Marshall DJ (2020) Metabolic rate, context-dependent selection, and the competition-colonization trade-off. Evolution LettersPDFDOI
Lab life has, of necessity, been curtailed throughout the world but it has provided an opportunity for researchers to spend time trawling the literature for data to use in meta-analyses. Our lab is no different and so in this edition of lab life we aim to give an overview about what some of our members have been working on.
One tricky element of this data collection has been converting the different body size measurements to mass. For example, a paper may present data on head width in wasps, hind tibia length in grasshoppers, or carapace lengths in crabs but Michaela needs to convert this to a measure of mass. To do this she has had to create a repository of morphometric allometries for a number of different species, another great resource for other meta analyses that the lab group might do in which body mass needs to be calculated.
A separate study is also underway that is looking at not only the number of offspring but the size of those offspring in relation to maternal size. So, Melanie Lovass, with help from Michaela, has been compiling data to enable Hayley Cameron and our (now virtual) visitor Darren Johnson from California State University to ask the question: do bigger mothers produce bigger and/or more offspring and are there any differences between warm-blooded and cold-blooded animals?
PhD student, Emily Richardson is particularly interested in organisms that have complex life histories or, in other words, go through metamorphosis to become adults. Emily is gathering data on growth rates in amphibians, fish and marine invertebrates to test the theory that growth rate is maximised relative to mortality rate at the time of metamorphosis, which would mean that fitness is increased.
George Jarvis and Sam Ginther are also doing meta-analyses that relate to their PhD projects. George, like Emily, is interested in organisms with complex life histories but he is looking at large scale evolutionary change in metabolic rate. For his meta-analysis he is compiling metabolic data from marine invertebrates and looking at how metabolic rates vary between species with different developmental modes. With this work, he hopes to better understand the evolution of metabolic rate in complex life cycles.
Sam is interested in the cost of reproduction. He is collecting data on metabolic rates in reproductive and non-reproductive adults as well as their offspring. This will help him understand how the energy used for reproduction affects the production of offspring in species with dramatically different life histories.
Louise Noergaard has just started a post doc in the CGB and is busy working on a collaborative project between Dustin Marshall and Beth McGraw from Penn State University. Louise is looking at the relationship between wing length and body mass in mosquitoes and assessing how these measures of size relate to lifetime reproductive output. This information can then be put into a model that will consider how these measures of size and reproductive output affect existing predictions of mosquito spread.
Authors: Emily J Lombardi, Candice L Bywater, and Craig R White
Published in:Journal of Experimental Biology
The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance.
The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea.
In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species.
Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N. cinerea, which raises further questions about the generality of the hypothesis.
Lombardi EJ, Bywater CL, White CR (2020) The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea. Journal of Experimental BiologyPDFDOI
We all know the expression “you are what you eat” but do juvenile diets determine your adult size or can adult diets change things? Gonçalo Poças, Alexander Crosbie and Christen Mirth have used a model organism – the fruit fly Drosophila melanogaster – to explore this question.
They found that while larval nutritional conditions play the dominant role in determining both adult body weight and appendage size in D. melanogaster, the adult diet can adjust body weight as the flies age.
The team manipulated both the quality and energy quantity of diets that larval and adult flies received in two experiments.
In the first experiment calorie content was held stable but the ratio of protein to carbohydrate was either 1:2 (high quality) or 1:10 (low quality). In the second experiment flies were fed a high quality diet but with two different calorie contents. The low calorie content diet was 25% of the high calorie diet.
Importantly, larvae were reared on one of the two diets in each experiment and then after “eclosing” (emerging as an adult) they either remained on the same diet or were switched to the alternative diet. This allowed the researchers to tease apart at what life-stage diet was most influential in determining measures of adult size.
Adult weights, wing area and femur size were measured at 3, 10 and 17 days old. The team predicted that adult weight would be more influenced by adult diet but that wing area and femur size would be determined by larval diet.
For the most part, the team found that the larval diet contributed more to differences in adult weight, wing area, and femur size in both males and females, but the quality of the larval diet had greater effects on adult size than the calorie content.
In addition to the effects of larval diet on adult size traits, Gonçalo and his colleagues found that animals subjected to poor larval nutrition were able to increase their body weight if maintained on good quality diets during the adult stages.
One surprising result the team uncovered was that the adult femur size changed with age, and depended on both the larval and adult diet. This suggests that the size of adult appendages might not be as fixed as previously thought.
So, to return to our initial question. Yes, the juvenile diet is very important in determining measures of adult size, but adult diets can make up for nutritional deficiencies in earlier life to some extent – in fruit flies at least.
Understanding how energy is used (or not used) in individuals, populations and communities has fascinated biologists for many years. Giulia Ghedini, an Australian Research Council research fellow in the Centre for Geometric Biology, is particularly interested in how communities use energy. Giulia and her colleagues have found that older communities of marine phytoplankton waste less energy than new or early successional communities.
In a previous post, we described how Giulia and her colleagues used marine invertebrates to test whether ‘older’ communities minimised energy wastage as predicted by Robert MacArthur in 1969. MacArthur basically said that, due to competition for resources, a community of species will, over time, maximise the efficiency with which it consumes resources meaning that older communities have very little energy (resource) wastage.
If MacArthur was right, then we can better understand and predict how disturbances that change the age or successional stage of a community might impact community function and invasion risk. An older community might be able to sustain a greater biomass with the same resource requirements of a younger community. Not only that, but a community that efficiently uses all the energy or resources available makes it difficult for a new species to gain a foothold.
While the team found some support for MacArthur’s theory in their initial study, it was far from clear-cut and they thought that this might be because their experimental setup allowed for predation and immigration; MacArthur’s theory relates to a closed system where competition between species is the driving force for community structure and function.
To tackle this problem Giulia and her colleagues designed a new experimental setup using a completely different system: marine phytoplankton. They were able to create ‘starter’ assemblages of phytoplankton in the lab. They used six species and then followed these assemblages through time measuring energy inputs (light and nutrients) and energy use (photosynthesis, metabolism and overall production). This allowed them to work out how much energy from resources was not used and how much was lost to maintenance – metabolism and mortality – the two components of MacArthur’s ‘wastage’. They also tracked changes in species composition and the size structure of the communities to understand their links with energy wastage.
The team found some marked changes in the phytoplankton communities. Larger species became more dominant over time and this was consistent in all 20 of the experimental communities. Surprisingly, neither changes in dominant species nor the homogenisation of communities were driving changes in energy flux.
So, while the composition of the species changed in a consistent way as the communities ‘aged’, the functioning of communities tracked less consistently, meaning that the oldest communities were not necessarily the most energy efficient. But there was a general pattern that fitted with MacArthur’s prediction that older more established communities would minimise energy wastage. And, as predicted, the changes were due to the two components of energy use changing in opposite directions.
The combined results from the team’s work suggest that overall patterns in community function might be predictable over time and that MacArthur’s minimisation principle might apply across very different systems.
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.
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.
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.
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?
Authors: Dustin J Marshall, Amanda K Pettersen, Michael Bode, and Craig R White
Published in:Nature Ecology & Evolution
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 & EvolutionPDFDOI