Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Authors: Martino E Malerba, Dustin J Marshall, Maria M Palacios, John A Raven, and John Beardall

Published in: New Phytologist

Summary

Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume‐specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2‐concentrating mechanisms (CCMs).

Previous studies have focused on among‐species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3‐fold difference in cell volume. We compared CO2affinity, external carbonic anhydrase (CAext), isotopic signatures (δ13C) and growth among size‐selected lineages.

Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13C. Larger cells also achieved faster growth and higher maximum biovolume densities.

We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

Malerba ME, Marshall DJ, Palacios MM, Raven JA, Beardall J (2020) Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New Phytologist PDF DOI

Winners and losers: why developmental strategy is important in determining marine invertebrate distributions under future climate

Global change will alter the distribution of organisms around the planet. Dustin Marshall and Mariana Álvarez-Noriega found rising ocean temperatures will impact early life stages of marine invertebrates and change the patterns in the distribution of species that we see today. In particular, species in which mothers invest heavily in offspring will be the biggest losers. These species occur predominantly at the poles.

In terrestrial environments seeds often disperse in the wind, with shape and size affecting how far they travel. It turns out much the same happens in the ocean but currents rather than wind carry marine larvae to their new homes. Larvae able to feed spend much longer in the water column meaning these species have far greater dispersal capabilities.

As with plants, dispersal is crucial to the survival of marine populations. Arriving larvae can seed new areas, re-seed vulnerable populations, and provide genetic variation for subsequent generations in far-flung regions. There is a downside: if temperature affects dispersal, it will also shape how species are affected by global warming.

Not all marine species use the same reproductive or life-history strategies which can mean differences in dispersal distances from centimetres to hundreds of kilometres for different species. Interestingly, there is a well-recognised relationship between latitude (or temperature) and reproductive strategy.

Species at higher latitudes (nearer the poles) tend to invest more heavily in their offspring and produce non-feeding larvae or bypass the larval stage altogether. This means these species don’t disperse very far. In contrast, tropical species tend to put little effort into provisioning their offspring and produce larvae that can feed. As a result, these larvae can spend a lot more time in the plankton and can be dispersed vast distances.

Dustin and Mariana wanted to know how these dispersal relationships might change as global temperatures change. To address this question, they revisited the database of marine invertebrates classified into feeding / development types from a previous study. They established relationships between temperature and development mode so they could then explore how predicted temperatures for 2100 would change patterns in distributions.

So, how will global warming affect these relationships? We know species’ in warmer waters are more likely to produce large numbers of feeding larvae able to remain in the water column for weeks at a time. As waters warm, these species are well placed to extend their range.

In contrast, species based in cooler waters tend to invest heavily in individual offspring, meaning that they develop quicker and settle closer to their parents. This reproductive strategy means that such species are more vulnerable to rapid global change as moving to new areas will, of necessity, be step-wise and slow.

Species at the poles will therefore be the biggest losers because not only will their lower dispersal lifestyles mean they will be slow to access cooler waters but also the options are limited; there is nowhere to go.

This figure shows the predicted change in prevalence of three different development modes in the southern hemisphere under a predicted scenario for global warming. The blue line shows an even increase of feeding larvae across all latitudes, while non-feeding planktonic larvae (purple line) will only increase at higher latitudes and there will be a loss of species that invest most heavily in their young and don’t have a planktonic larval stage near the poles (orange line).

This research was published in the journal Philosophical Transactions of the Royal Society B: Biological Sciences.

Projecting marine developmental diversity and connectivity in future oceans

Authors: Dustin J Marshall and Mariana Álvarez-Noriega

Published in: Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Global change will alter the distribution of organisms around the planet. While many studies have explored how different species, groups and traits might be re-arranged, few have explored how dispersal is likely to change under future conditions.

Dispersal drives ecological and evolutionary dynamics of populations, determining resilience, persistence and spread. In marine systems, dispersal shows clear biogeographical patterns and is extremely dependent on temperature, so simple projections can be made regarding how dispersal potentials are likely to change owing to global warming under future thermal regimes.

We use two proxies for dispersal — developmental mode and developmental duration. Species with a larval phase are more dispersive than those that lack a larval phase, and species that spend longer developing in the plankton are more dispersive than those that spend less time in the plankton.

Here, we explore how the distribution of different development modes is likely to change based on current distributions. Next, we estimate how the temperature-dependence of development itself depends on the temperature in which the species lives, and use this estimate to project how developmental durations are likely to change in the future.

We find that species with feeding larvae are likely to become more prevalent, extending their distribution poleward at the expense of species with aplanktonic development. We predict that developmental durations are likely to decrease, particularly in high latitudes where durations may decline by more than 90%. Overall, we anticipate significant changes to dispersal in marine environments, with species in the polar seas experiencing the greatest change.

This article is part of the theme issue ‘Integrative research perspectives on marine conservation’.

Marshall DJ, Álvarez-Noriega M (2020) Projecting marine developmental diversity and connectivity in future oceans. Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI

Surviving starvation: feeding is not imperative to complete larval development for the copepod Tisbe sp.

Marine invertebrates display a range of complex life-history strategies. In general, larvae fall into one of two groups. They either meet the nutritional requirements of development by feeding during the larval phase or, they depend on nutrients supplied by the mother. Very rarely they can do both. These so-called ‘facultative feeders’ get a benefit from feeding but can, if necessary, complete larval development without food.

Alex Gangur and supervisor Dustin Marshall have found that a small crustacean can be added to this relatively short list of species that incorporate facultative feeding into the larval stage. Alex uses the copepod Tisbe sp. as his model species in a series of long-term experiments but he was surprised when he noticed that some of the larvae seemed to survive without food.

Alex and Dustin designed a series of experiments to determine if Tisbe was indeed a facultative feeder and, if so, what was the cost of completing development without food? They were also interested in how temperature might affect the outcomes as temperature is well known to have a strong relationship with larval development.

They set up a series of experiments where newly hatched larvae were assigned to vials with or without food and to one of two temperatures and individuals were monitored through metamorphosis and until they reproduced or died.

They found that a proportion of the starved copepods not only survived but went on to reproduce. But there was a cost. Development time was much longer in starved copepods compared to those that were fed and a higher temperature reduced development time in both feeding and starved copepods. The size of juveniles immediately after metamorphosis was smaller in starved copepods.

Starved copepods had reduced survival, longer development times and were smaller immediately after metamorpohosis.

Surprisingly, there was little carryover of the larval experience in the time to maturity or reproductive effort. Instead, the amount of food received as a juvenile was more important. But, more work is needed on the impacts of larval starvation on adult performance and, in particular, the effects of larval starvation on lifetime reproductive rate.

It is always difficult to extrapolate from lab experiments to real-world situations but the ability to complete larval development and metamorphosis in the absence of food likely provides an important buffer to populations experiencing fluctuating food availability.

This research is published in the journal Marine Ecology Progress Series.

Dietary preferences in filter-feeding animals might explain their crowded co-existence

An enduring concept in ecology is that space is the resource most in demand for communities living on hard substrates such as rocky shores and pier pilings. We have seen before how these communities can be extremely dense and diverse with little or no unoccupied space. But is space the whole story? These communities also need food and oxygen. How do such dense assemblages of animals manage to extract enough food to allow them to co-exist?

Belinda Comerford, Mariana Álvarez-Noriega, and Dustin Marshall have found different species of filter-feeders tend to consume one species of phytoplankton much more than others when offered a selection. They noticed studies looking at the role food plays in structuring filter-feeding communities tend to consider phytoplankton as a uniform resource. This makes no allowance for differences in size, shape or chemical make-up of the different algal species.

Belinda, Mariana and Dustin suspected that different species of filter-feeders will consume different components of the phytoplankton, reducing competition for food and allowing for the dense and diverse communities that we see in nature. So, they set about testing how different species of filter feeder consumed a mix of three different phytoplankton species that varied in size and shape and chemical make-up. 

They used 11 different species of invertebrate filter-feeding animals and offered them a mix of the three phytoplankton species. They measured the concentrations of each phytoplankton species in the animal chambers one minute and one hour after adding equal volumes of each species to the chambers. They also had control chambers that contained no animals which enabled them to estimate how much of the algae settled out to the bottom during the experimental period.

While most of the animals ingested all three phytoplankton species they did so at different rates. The encrusting bryozoan Watersipora subtorquata consumed the largest algal species at a much greater rate than it did the other two species while the sponge Sycon spp. favoured the smallest algal species. Some species such as the sea squirt Ciona intestinalis appear to be generalists, consuming all three algal species at the same rate. 

It seems that Belinda, Mariana and Dustin might be right. Thinking of phytoplankton as a homogenous resource underestimates the potential for reducing competition between filter-feeding species. If, instead of competing for a ‘common pool’ of phytoplankton, filter feeders target specific subsections then the diverse and densely packed communities that we see are more readily explained.

This research is published in the journal Oecologia.

The different invertebrates ingested the different phytoplankton species at different rates.

Is the X chromosome a hot spot for sexually antagonistic polymorphisms? Biases in current empirical tests of classical theory

Authors: Filip Ruzicka and Tim Connallon

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Females and males carry nearly identical genomes, which can constrain the evolution of sexual dimorphism and generate conditions that are favourable for maintaining sexually antagonistic (SA) polymorphisms, in which alleles beneficial for one sex are deleterious for the other.

An influential theoretical prediction, by Rice (Rice 1984 Evolution), is that the X chromosome should be a ‘hot spot’ (i.e. enriched) for SA polymorphisms. While important caveats to Rice’s theoretical prediction have since been highlighted (e.g. by Fry 2010 Evolution), several empirical studies appear to support it.

Here, we show that current tests of Rice′s theory—most of which are based on quantitative genetic measures of fitness (co)variance—are frequently biased towards detecting X-linked effects. We show that X-linked genes tend to contribute disproportionately to quantitative genetic patterns of SA fitness variation whether or not the X is enriched for SA polymorphisms.

Population genomic approaches for detecting SA loci, including genome-wide association study of fitness and analyses of intersexual FST, are similarly biased towards detecting X-linked effects. In the light of our models, we critically re-evaluate empirical evidence for Rice′s theory and discuss prospects for empirically testing it.

Ruzicka F, Connallon T (2020) Is the X chromosome a hot spot for sexually antagonistic polymorphisms? Biases in current empirical tests of classical theory. Proceedings of the Royal Society B: Biological Sciences PDF DOI

Food and chemical cues can both drive changes in metabolic rates

Metabolic rate, or energy use, changes with the size of the organism. This general pattern has been observed across different species, as well as among individuals of the same species. But while the broad pattern holds, individuals of the same species and the same size can also vary in the amount of energy they use.

Some studies have shown that individuals have lower metabolic rates as population numbers go up, but no one really knows why. Metabolic rates increase following food intake, so one plausible explanation is that competition for food in crowded conditions reduces food intake and, in turn, metabolic rates.

Melanie Lovass and her supervisors Dustin Marshall and Giulia Ghedini have run a series of experiments to investigate this possibility.

The team used the model species Bugula neritina to test their ideas. They ran a series of experiments where they were able to measure metabolic rates in individual Bugula colonies and they manipulated food, oxygen concentration, water flow and chemical cues to try and tease apart what was causing a reduction in metabolic rates in dense populations.

In the model system, each of these measures are influenced by how sparse or dense the population is. As expected, food availability affected metabolic rates but the team was surprised to find that chemical cues from individuals of the same species are also able to drive changes in metabolic rates.

Metabolic rates were lower in colonies that were starved, but metabolic rates were not affected by changes in water flow and oxygen concentrations.

This graph shows metabolic rates for <em>Bugula<em> colonies that have been exposed to chemical cues from other colonies (red) are lower than metabolic rates for the control colonies (blue).

More interestingly, Melanie and her supervisors found that metabolic rates were suppressed in Bugula colonies that were kept in ‘pre-conditioned’ water. This water had been exposed to other Bugula colonies overnight and so incorporated any chemical cues released from these other colonies. Melanie thought that chemical cues from fellow colonies might signal a reduction in feeding rates. To check if this was the case, she counted the number of feeding structures active in colonies exposed to ‘pre-conditioned’ versus normal seawater.

They found no differences in feeding rates indicating that the chemical cues from Bugula colonies were suppressing physiological processes rather than reducing feeding rates. So, while the chemical cues from other Bugula colonies reduce energy use, this reduction is in processes other than feeding activity.

While searching for food is energetically costly; keeping up feeding activity may be worth the costs and become even more important when access to food is very competitive.

Bugula are colonial organisms made up of ‘modules’. Each module has its own feeding structure – a crown of tentacles – known as a lophophore. There was no difference in the number of active lophophores in the colonies exposed to chemical cues compared to the control colonies. Photo credit: Amy Hall.

This research is published in the Journal of Experimental Biology.

Estimating energy use in communities

As ecologists, we often want to get an idea of how a community functions. For example, how much food does a community of animals consume every day? Or how much oxygen do plants produce every day? We can get an idea of these functions by measuring the energy use (or metabolism) of a community. But such functional measures can be difficult to collect, especially for an entire community. 

Since a community is made up of many species, estimating the total metabolism from the metabolism of each species separately is a way around this problem. But the methods we use, and the data required, vary and may not be validated against actual data because these are rarely available. 

Giulia Ghedini, Martino Malerba and Dustin Marshall have set out to test six different ways of estimating the energy use of a community. The authors measured actual metabolic rates in communities of phytoplankton (tiny marine microalgae) seeded with six different species of various sizes and left to change through time.

Previous work from the CGB meant the team had all the information they needed to estimate community energy use for the six methods. The different methods are summarised below.

There are a number of different ways we can estimate community metabolism that vary in complexity.

It turns out that when we are interested in whole community metabolism, size doesn’t matter. Why? Because larger species tend to be less abundant within communities, so even if each of them consumes more energy, the total energy use remains the same because there are fewer of them. While we knew this was the case for well-established communities, this new work shows that it is also true for communities as they change through time.

What is more, the team found that, in communities, the usual relationship between size and metabolism changed. Metabolism usually increases with size, but to a lesser extent for larger organisms (this is called an allometric relationship). This study showed that when measured across all species in the community, this relationship changed and the average energy use of species increased in direct proportion to their average size (this is an isometric relationship). This is why we can predict the total metabolism from the energy use per unit biomass. 

But towards the end of the experiment, when communities were dominated by larger cells, this ‘perfectly proportional’ relationship broke down. Giulia and her colleagues think that, when large species are very abundant, they suffer more from competition and reduce their metabolism more than smaller species. 

So, the good news is that we may be able to estimate community energy from easy to collect biomass data, but first, we need to see if this result applies to different communities. We also need more studies on how competition affects energy use, as the results from this study suggest they are important drivers of energy flow.

All of the methods are based on underlying theory so testing which methods are best at estimating actual metabolism can help us understand how energy use works in communities. This figure summarises what theory predicts we should have found compared to what we actually found.

This research was published in Proceedings of the Royal Society B: Biological Sciences.

How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux

Authors: Giulia Ghedini, Martino E Malerba, and Dustin J Marshall

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Size and metabolism are highly correlated, so that community energy flux might be predicted from size distributions alone. However, the accuracy of predictions based on interspecific energy–size relationships relative to approaches not based on size distributions is unknown.

We compare six approaches to predict energy flux in phytoplankton communities across succession: assuming a constant energy use among species (per cell or unit biomass), using energy–size interspecific scaling relationships and species-specific rates (both with or without accounting for density effects).

Except for the per cell approach, all others explained some variation in energy flux but their accuracy varied considerably. Surprisingly, the best approach overall was based on mean biomass-specific rates, followed by the most complex (species-specific rates with density).

We show that biomass-specific rates alone predict community energy flux because the allometric scaling of energy use with size measured for species in isolation does not reflect the isometric scaling of these species in communities. We also find energy equivalence throughout succession, even when communities are not at carrying capacity.

Finally, we discuss that species assembly can alter energy–size relationships, and that metabolic suppression in response to density might drive the allometry of community energy flux as biomass accumulates.

Ghedini G, Malerba ME, Marshall DJ (2020) How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux. Proceedings of the Royal Society B: Biological Sciences PDF DOI

Cell size, genome size and the selfish gene

Classic theories such as the ‘selfish gene hypothesis’ are not always easy to test. If true, then the theory proposes that cells accumulate extra DNA over time even when they provide no benefit to the organism – selfish genes. This means individuals with more DNA relative to their cell size should have reduced fitness. What is more, because the accumulation of DNA creates a burden on the organism, a good evolutionary strategy should be to reduce the amount of redundant DNA over time.

In one of the first tests of the theory using a single species, Martino Malerba, Giulia Ghedini and Dustin Marshall have found direct evidence that reduced amounts of total DNA (genome size) is associated with fitness benefits in a species of marine microalgae.

Scientists face a problem when they compare cell size and genome size between different species. It is hard to separate whether the slower rates of metabolism, development and growth are a result of genome size or the fact that larger organisms tend to have a slower pace of life anyway.

Martino and his colleagues were able to overcome this issue by using their evolved lines of the marine phytoplankton Dunaliella tertiolecta where cells have been artificially selected to be large or small. They were able to use a staining technique to measure the amount of DNA content within cells of different sizes but, importantly, of the same species and the same evolutionary age.

They weren’t surprised to find larger cells had more DNA. But they also found that, in cells of the same size, the cells with smaller genomes grew faster and accumulated more biomass; that is, had greater fitness.

So, this first finding was consistent with the prediction that reducing the amount of DNA in a cell can have positive effects for the fitness of a species. But having demonstrated that minimizing DNA can improve fitness, the team then wanted to test the prediction that species should decrease their DNA content as they evolve. Again, they were able to test this by using the Dunaliella and monitoring the evolving lines for a year or approximately100 generations.

Their results confirmed that cells decreased their DNA content by up to 11% across 100 generations of evolution. However, they also found that cells with already low amounts of DNA showed no change over time, which suggests the existence of an absolute lower limit in the DNA content of this species.

Overall, they have direct evidence for fitness benefits associated with reduced relative genome size consistent with the selfish gene hypothesis and as well as a minimum genome size below which an organism can’t maintain functionality.

This figure looks at how genome size or cell DNA content changes with cell size. The continuous black line shows the relationship between the two for the large, small and control algae after 350 generations of evolution. The broken line shows the relationship after 450 generations of evolution – 1 year later. Notice how the cell DNA content has reduced after 1 year of evolution.

This research was published in the journal Current Biology.