Testing the drivers of the temperature-size covariance using artificial selection

Authors: Martino E Malerba, and Dustin J Marshall

Published in: Evolution

Abstract

Body size often declines with increasing temperature. Although there is ample evidence for this effect to be adaptive, it remains unclear whether size shrinking at warmer temperatures is driven by specific properties of being smaller (e.g., surface to volume ratio) or by traits that are correlated with size (e.g., metabolism, growth).

We used 290 generations (22 months) of artificial selection on a unicellular phytoplankton species to evolve a 13‐fold difference in volume between small‐selected and large‐selected cells and tested their performance at 22 °C (usual temperature), 18 °C (−4), and 26 °C (+4).

Warmer temperatures increased fitness in small‐selected individuals and reduced fitness in large‐selected ones, indicating changes in size alone are sufficient to mediate temperature‐dependent performance.

Our results are incompatible with the often‐cited geometric argument of warmer temperature intensifying resource limitation. Instead, we find evidence that is consistent with larger cells being more vulnerable to reactive oxygen species. By engineering cells of different sizes, our results suggest that smaller‐celled species are pre‐adapted for higher temperatures.

We discuss the potential repercussions for global carbon cycles and the biological pump under climate warming.

Malerba ME, Marshall DJ (2019) Testing the drivers of the temperature-size covariance using artificial selection. Evolution PDF DOI

Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology

Authors: Evatt Chirgwin, Dustin J Marshall, and Keyne Monro

Published in: Functional Ecology

Abstract

Global warming may threaten fertility, which is a key component of individual fitness and vital for population persistence. For males, fertility relies on the ability of sperm to collide and fuse with eggs; consequently, sperm morphology is predicted to be a prime target of selection owing to its effects on male function.

In aquatic environments, warming will expose gametes of external fertilizers to the physiological effects of higher temperature and the physical effects of lower viscosity. However, the consequences of either effect for fertility, and for selection acting on sperm traits to maintain fertility, are poorly understood.

Here, we test how independent changes in water temperature and viscosity alter male fertility and selection on sperm morphology in an externally fertilizing marine tubeworm. To create five fertilization environments, we manipulate temperature to reflect current-day conditions (16.5 °C), projected near-term warming (21 °C) and projected long-term warming (25 °C), then adjust two more environments at 21 °C and 25 °C to the viscosity of environments at 16.5 °C and 21 °C, respectively. We then use a split-ejaculate design to measure the fertility of focal males, and selection on their sperm, in each environment.

Projected changes in temperature and viscosity act independently to reduce male fertility, but act jointly to alter selection on sperm morphology. Specifically, environments resulting from projected warming alter selection on the sperm midpiece in ways that suggest shifts in the energetic challenges of functioning under stressful conditions. Selection also targets sperm head dimensions and tail length, irrespective of environment.

We provide the first evidence that projected changes in ocean temperature and viscosity will not only impact the fertility of marine external fertilizers, but expose their gametes to novel selection pressures that may drive them to adapt in response if gamete phenotypes are sufficiently heritable.

Chirgwin E, Marshall DJ, Monro K (2019) Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Functional Ecology PDF DOI

Size and density mediate transitions between competition and facilitation

Authors: Hayley Cameron, Tim Coulson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Species simultaneously compete with and facilitate one another. Size can mediate transitions along this competition–facilitation continuum, but the consequences for demography are unclear.

We orthogonally manipulated the size of a focal species, and the size and density of a heterospecific neighbour, in the field using a model marine system. We then parameterised a size‐structured population model with our experimental data.

We found that heterospecific size and density interactively altered the population dynamics of the focal species. Size determined whether heterospecifics facilitated (when small) or competed with (when large) the focal species, while density strengthened these interactions.

Such size‐mediated interactions also altered the pace of the focal’s life history. We provide the first demonstration that size and density mediate competition and facilitation from a population dynamical perspective. We suspect such effects are ubiquitous, but currently underappreciated.

We reiterate classic cautions against inferences about competitive hierarchies made in the absence of size‐specific data.

Cameron H, Coulson T, Marshall DJ (2019) Size and density mediate transitions between competition and facilitation. Ecology Letters PDF DOI

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

How can pathogens optimise both transmission and dispersal?

Certain pathogens (disease-producing organisms) are stuck in a Catch-22; to survive they need to continue to find, and infect, new hosts. But infection makes their hosts sick and less likely to move to where there are new hosts to infect.

PhD student Louise Nørgaard and her supervisors Ben Phillips and Matt Hall have found evidence of a pathogen that resolves this issue by exploiting the differences in size and behaviour of male and female hosts to optimize its own chance of successful infection.

The team uses the freshwater crustacean Daphnia magna and its common pathogen Pasteuria ramosa as a model system to test the idea that a pathogen can exploit differences between the sexes of a host to its advantage. The pathogen P. ramosa is ingested by Daphnia after which it sterilises and kills the host, releasing transmission spores that are ready to infect a new host. Female Daphnia are bigger, live longer and are more susceptible to infection than males.

Louise set up two separate experiments, allowing her to monitor the probability that Daphnia would disperse from a crowded area to a less crowded area and to measure the rate and distance travelled by infected and uninfected male and female individuals.

In the first experiment Louise was able to capitalise on previous work that has shown that Daphnia will disperse when conditions are crowded. Exposure to water taken from high densities of Daphniais enough to encourage dispersal. Louise used ‘crowded-conditioned’ water and found infected male Daphnia were more likely to disperse than uninfected males. Infected females, on the other hand, were a lot less likely to disperse than uninfected females.

A second experiment found that infected females had four times the number of transmission spores than infected males and moved less far and more slowly than males or uninfected females. Infected males though, moved at the same rate and travelled the same distance as uninfected males.

The figure A shows how far male (blue) and females (green) disperse when infected with the pathogen compared to uninfected individuals. Louise tested two types of pathogen C1 and C19. She also measured the distance travelled (B) and the spore load in infected individuals (C).

So how do these differences between the sexes help the pathogen? Females are bigger and can host large numbers of transmission spores. Staying put when densities are high means they are releasing this large number of spores into a crowd – potentially maximising the chance of further infections.  Smaller males have fewer spores to release and the chance of secondary infections may be maximised when they move to new areas where few individuals are already infected.

Importantly the differences in dispersal behaviour between infected males and females seem to relate directly to the way the pathogen interacts with each sex. Uninfected males and females had similar rates and distance of dispersal while uninfected females were more likely to move away from crowded habitats than males. These patterns disappear when both sexes are infected.

Do these different infection strategies in different sexes provide a form of bet-hedging for the pathogen? Louise and her supervisors think they do and, if widespread, will have important implications for disease dynamics.

This research is published in the journal Biology Letters.

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).

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.