Plastic responses to changes in environment are not necessarily adaptive

Phenotypic plasticity is a term familiar to evolutionary biologists. It refers to the ability of an organism to respond to a changing environment by changing its physical properties – its phenotype. For example, metabolic rate changes with temperature and resource availability.

We usually assume that such changes are adaptive, that is, changes are in the same direction as selection and so will increase the fitness (reproductive output) of the organism in that environment. But, importantly, we don’t usually test for the adaptive significance of phenotypic plasticity because we don’t typically estimate selection in different environments when we assess plasticity.

Lukas Schuster and his supervisors, Craig White and Dustin Marshall, used the model species Bugula neritina to investigate whether changes in metabolic rates in response to different field environments are an example of adaptive phenotypic plasticity. To their surprise they found that, while Bugula exhibited plasticity in metabolic rate, it was not adaptive.

Bugula is a small filter feeding colonial bryozoan that is often found on the undersides of piers. It is also found on vertical surfaces such as pier pilings, although the increased UV radiation and sedimentation experienced on vertical surfaces combine to make this a more stressful living environment.

Lukas collected mature colonies of Bugula from the field and then spawned them in the laboratory and settled the larvae onto small acetate sheets. This allowed Lukas to deploy the Bugula on vertically or horizontally suspended panels (corresponding to harsh and benign environments respectively) and to return colonies to the laboratory to measure metabolic rates. They did two experimental runs to test the consistency of the results.

As a first step, Lukas and his supervisors had to determine how selection on metabolic rate varies across harsh and benign environments. In other words, they needed to establish the relationship between metabolic rate and reproductive output (fitness) in each environment.

They deployed newly settled Bugula to a common, benign environment for three weeks before returning these colonies to the laboratory to measure metabolic rates. Half of the colonies were then deployed into the harsh environment and half was kept in the benign environment. Growth, survival and lifetime reproductive output were then tracked for each colony; this allowed the team to determine whether there was any fitness advantage associated with particular metabolic rates in each environment.

Surprisingly, they found no differences in selection on metabolic rates in the two environments. Instead, in one experimental run, they found evidence that smaller individuals with lower metabolic rates and larger individuals with higher metabolic rates went on to produce more offspring in both environments. This suggests that metabolic rate is unlikely to evolve independently of other traits.

To measure plasticity Lukas returned all colonies to the laboratory to measure metabolic rates for a second time. Colonies from the harsh environment had overall lower metabolic rates compared to colonies from the benign environment.

In the first experimental run the team found that smaller individuals with lower metabolic rates and larger individuals with higher metabolic rates went on to produce more offspring (red areas in graph) regardless of the environment they were in.
In the first experimental run the team found that smaller individuals with lower metabolic rates and larger individuals with higher metabolic rates went on to produce more offspring (red areas in graph) regardless of the environment they were in.

Given the strong and consistent metabolic response to the different environments that the team observed, it would have been tempting to infer that such a response increases fitness. While this seems intuitive, it is not consistent with what they know about selection on metabolic rate in the different environments. There was no difference in the relationship between metabolic rates and reproductive outputs in the two environments and so, although the changes they saw in metabolic rate with environment show that metabolic rate is plastic, their results show that such plasticity is not always adaptive.

Lukas and his supervisors emphasise the importance of assessing selection on a trait in the different environments before assuming that ‘plastic’ responses to different environments are necessarily adaptive. Instead, metabolic plasticity may merely represent a passive response due to correlations with other traits or there may be limits to physiological plasticity due to biochemical constraints. Nonetheless, further studies are needed in order to understand the drivers and consequences of metabolic plasticity in the field.

This research was published in the journal Oikos.

Female advantage to heat stress is negated by exposure to a pathogen

Increasing temperatures are not the only changes we can expect with future climate. The prevalence of infectious disease is also predicted to increase. The persistence of organisms will depend not only on their thermal tolerance but also how well they fight infection. Not all individuals do both these things well.

Males and females differ in many characteristics, from body size to behaviour, and it may be that each sex will also vary in how well they cope with both thermal stress and infection. Yet this question has been neglected up until now. Tess Laidlaw and her colleagues have used a model system to address this gap. In their system they found that females had a higher upper limit of thermal tolerance than males but, when infected with a pathogen, this difference disappeared.

The model system consists of a small aquatic crustacean, Daphnia magna and a common bacterial pathogen, Pastueria ramosa. Using multiple host and pathogen strains, the team exposed Daphnia to one of the pathogens or left them unexposed as controls. They then subjected male and female Daphnia from the different treatments to acute heat stress that is lethal to the animals and recorded the time to immobilisation – known as the knockdown time. Knockdown times measure the capacity of an individual to avoid physical incapacitation during temperature extremes and are a common measure of assessing thermal limits.

They weren’t surprised to find that females were more heat resistant than males. Sexual differences in heat tolerance have been found in other species, and the teams’ findings were consistent with differences in knockdown times for Daphnia collected from a range of latitudes. The greater tolerance of female Daphnia to heat stress is important because females invest more in their offspring. This means that population growth is likely to be more strongly linked to female survival than male survival.

Once infected however, any advantage the females demonstrated in tolerating heat stress was lost. Knockdown times in males and females were now markedly similar. Tess and her colleagues have shown how the introduction of a pathogen can potentially negate any buffer that the higher thermal limits of females provide for a population.

For the two different strains of the host Daphnia magna females showed more resistance to heat than males. But once infected with a pathogen there was little difference in knockdown times between males and females.

This research was published in the journal Ecology and Evolution.

Hot spots on the X chromosome? Testing a classic theory of sexual antagonism

Biologists have long been interested in sexually antagonistic selection, in which the genetic variants that provide an advantage for one sex are disadvantageous for the other. Sexual antagonism is important because it helps maintain genetic variation and represents one of several ways in which populations might remain maladapted with respect to their environments.

In 1984, a theoretical prediction was proposed by William Rice that said the X chromosome should be a ‘hot spot’ for sexually antagonistic genetic polymorphism. His mathematical models indicated that sexually antagonistic alleles were more likely to remain polymorphic when they were linked to the X chromosome than when they were on other types of chromosomes (i.e., autosomes). Rice’s prediction that polymorphism is easier to maintain on the X chromosome critically depends on the dominance relations between sexually antagonistic alleles. Other researchers have shown that the autosomes are more conducive to maintaining genetic variation under conditions that differ from Rice’s assumptions.

There have been numerous empirical studies that have demonstrated apparent support for Rice’s theory. But Filip Ruzicka and Tim Connallon argue that these studies share a common but incorrect assumption: that signals from sexually antagonistic genetic variation are equally detectable whether the variation is on sex chromosomes (ie X-linked) or on autosomes.

Instead, Filip and Tim found that the existing methods for testing this classic theory are all biased towards finding signals of sexually antagonistic variation on the X chromosome. They developed mathematical models to test how much X chromosomes and autosomes contributed to signals of sexual antagonism and found a considerable bias in existing studies.

When they revisited the experimental studies using their models, they found that most of them were actually consistent with scenarios in which the X chromosome is not a hot spot for sexually antagonistic polymorphism.

Drosophila melanogaster, the common fruit fly, is often used as a model system to study sexual antagonism. Image credit: Francisco Romero Ferrero via Wikimedia Commons

So how can we be sure whether William Rice’s theory is correct or not? Filip and Tim concede that experimentally testing this classic theory is difficult. They suggest the most feasible approach is to compare fitness components between fathers and sons (who do not inherit their fathers X chromosome) with fitness components between fathers and daughters (who do). Modern genomic approaches that directly estimate the fitness effects of individual genetic variation (genome-wide association studies or “GWAS” of fitness) are also promising avenues for testing the theory.

Filip and Tim hope that their predictions provide better guidelines for future tests. Their models can be used as baseline expectations against which experimental data can be compared.

While they acknowledge that there are limitations in their models, they maintain further attention to this issue will greatly improve our ability to predict the potential contributions of X-linked and autosomal genes to population genetic diversity and species divergence.

This research is published in the journal Proceedings of the Royal Society B: Biological Sciences

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.