How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J Marshall, Carla M Sgrò, and Keyne Monro

Published in: Proceedings of the Royal Society B

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change?, Proceedings of the Royal Society B PDF DOI

Death is not the end, especially if you are a colonial organism

Colonial, or modular, organisms are fascinating because each module can experience its own life history while the colony as a whole shares resources. This means that when a module dies it can actually be beneficial to the whole colony. The death of an older module can mean resources are allocated to younger, more vital modules which, in turn, can increase colony reproduction and hence colony fitness. 

Most of our knowledge about these types of organisms comes from plants and although there are many marine examples of colonial organisms, there has been little testing of ideas about module mortality and its effects on colony fitness in these animals.

Karin Svanfeldt and her PhD supervisors Keyne Monro and Dustin Marshall have been working to redress the balance. Karin has been studying the colonial bryozoan Watersipora subtorquata as part of her PhD and she was interested in testing some ideas about selection on module longevity in this species and seeing how it compared with what we know about plants.

Karin used un-analysed data from a field experiment where she had manipulated food availability and flow rate. Karin also used data from another experiment where competition between different species was manipulated by settling Watersipora on either bare PVC plates or on plates where other animals were already growing.

Modules in colonial animals are called zooids and in the bryozoan Watersipora, growth and new zooids appear at the edge of the colony. Over time, the zooids in the centre of the colony lose colour and irreversibly senesce. Zooid senescence is visible as the appearance of a grey inner circle of older, dead zooids that expands as the colony grows. This meant that Karin was able to track individual zooids over time to provide measures of zooid longevity and also get data on the reproductive output of colonies to use as a measure of colony fitness. Karin measured reproductive output as either the number of new zooids or the number of ovicells per colony.

This data enabled Karin and her supervisors to ask the question: “does having a shorter zooid lifespan mean increased fitness for the colony as a whole?” Or, put another way: “is module longevity under selection?”

They found that, ‘Yes’ module longevity is under selection and that the strength of selection varies with environmental conditions, which is what has been found in numerous studies looking at modular plant species. 

This research has been published in the Journal of Evolutionary Biology.

Can we predict egg size of marine fish by looking at the predictability of the environment?

The size of eggs in marine fish has been observed to decrease with increasing temperatures and results from a new study support this finding but, more interestingly, suggest that the predictability of the environment is also important in shaping patterns in egg size.

Diego Barneche and Dustin Marshall from the Centre for Geometric Biology have collaborated with Scott Burgess of Florida State University to compile a dataset of 1078 observations of fish egg size taken from 192 studies that took place between 1880 and 2015 and which include 288 species. This enabled them to test multiple life history theories, including the prediction that in environments with stable food regimes the most effective strategy to maximise reproductive rates is to produce many small eggs.

When compiling this data, Diego and colleagues only included geo-located data so that they could use other existing datasets to estimate means and predictability of sea surface temperatures and chlorophyll a concentrations for the different locations.

The research team were interested, not only in testing how egg size responds to changes in average temperature, but how environmental productivity or food supply (using chlorophyll a as a proxy measure) will affect egg size. The team also formally tested how different components of environmental predictability would affect egg size; they looked at seasonality as well as temporal autocorrelation (how similar conditions at any one point in time are likely to be with previous conditions) to provide indices of environmental predictability.

Diego and colleagues found that egg size decreased as temperatures or chlorophyll a concentrations increased. In contrast, environments that were more seasonal in respect to temperature had larger eggs, but so did environments that were not seasonal in respect to chlorophyll a but were temporally autocorrelated.

These graphs show data from 192 studies and 1,078 observations of fish egg size where egg size decreased as both (a) temperature and (b) chlorophyll-a concentrations increased.

The findings from this study are consistent with a theory that suggests that in an unpredictable environment mothers employ a ‘bet-hedging’ strategy whereby they insulate their offspring from poor conditions through better provisioning, that is, they produce larger eggs.

Importantly this study demonstrated that different components of environmental variation – not just changes in the mean environmental state – contribute to observed patterns in egg size. As future changes to the ocean are expected to impact not only the average state but the degree of predictability, there may be profound effects on the distribution of marine life history traits.

This research is published in the journal Global Ecology and Biogeography

Global environmental drivers of marine fish egg size

Authors: Diego R Barneche, Scott C Burgess, and Dustin J Marshall

Published in: Global Ecology and Biogeography

Abstract

Aim: To test long‐standing theory on the role of environmental conditions (both mean and predictability) in shaping global patterns in the egg sizes of marine fishes.

Location: Global (50° S to 50° N).

Time period: 1880 to 2015.

Major taxa studied: Marine fish.

Methods: We compiled the largest geo‐located dataset of marine fish egg size (diameter) to date (n = 1,078 observations; 192 studies; 288 species; 242 localities). We decomposed sea surface temperature (SST) and chlorophyll‐a time series into mean and predictability (seasonality and colour of environmental noise – i.e. how predictable the environment is between consecutive time steps), and used these as predictors of egg size in a Bayesian phylogenetic hierarchical model. We test four specific hypotheses based on the classic discussion by Rass (1941), as well as contemporary life‐history theory, and the conceptual model of Winemiller and Rose (1992).

Results: Both environmental mean and predictability correlated with egg size. Our parsimonious model indicated that egg size decreases by c. 2.0‐fold moving from 1 to 30 °C. Environments that were more seasonal with respect to temperature were associated with larger eggs. Increasing mean chlorophyll‐a, from 0.1 to 1 mg/m3, was associated with a c. 1.3‐fold decrease in egg size. Lower chlorophyll‐a seasonality and reddened noise were also associated with larger egg sizes – aseasonal but more temporally autocorrelated resource regimes favoured larger eggs.

Main conclusions: Our findings support results from Rass (1941) and some predictions from Winemiller and Rose (1992). The effects of environmental means and predictability on marine fish egg size are largely consistent with those observed in marine invertebrates with feeding larvae, suggesting that there are important commonalities in how ectotherm egg size responds to environmental change. Our results further suggest that anthropogenically mediated changes in the environment will have profound effects on the distribution of marine life histories.

Barneche DR, Burgess SC, Marshall DJ (2018) Global environmental drivers of marine fish egg size, Global Ecology and Biogeography PDF DOI 

How does size affect the maintenance of a constant body temperature?

Staying warm is a subject close to many of our hearts during winter and we probably wouldn’t be surprised to hear that animals from colder climes have higher rates of energy expenditure.  But is this true for all species, or is it more complicated than that?

Researchers from Uruguay, Daniel Naya and Hugo Naya, have joined forces with Craig White from the Centre for Geometric Biology to investigate how body mass in mammals affects the relationship between energy expenditure and climate. They found that, yes, energy expenditure was greater for species that live in colder regions but only in mammals smaller than 100 g. The effect became less marked as the animals got bigger. 

The Basal Metabolic Rate (BMR) is a measure that represents the minimum amount of energy needed to maintain a relatively constant body temperature through active heat production.  It has been repeatedly demonstrated that there is a negative correlation between temperature and residual BMR in mammals and birds.

So where does body mass come into all this?  Over half of all mammals weigh less than 100 g although the range in body mass for mammals scales over 8 orders of magnitude. Also, smaller animals are generally easier to work with in the laboratory and so it is likely that much of our data on BMR in mammals comes from smaller species.

In order to untangle the effects of size on the ‘Temperature – BMR’ relationship, Daniel, Hugo and Craig looked at existing data on 458 mammal species. They compiled data on body mass, BMR and temperature from each collection site.  Their data set, as expected, included many more small species than big ones. What is more, their prediction that smaller species would be more dependent on adjustments in BMR to cope with lower temperatures, was confirmed.

There are other ways to maintain constant body temperatures apart from exerting more energy or increasing the Basal Metabolic Rate. Some examples include physiological adjustments, such as the separation of core and outer temperatures through peripheral vasoconstriction.  Behavioural adjustments, such as building / using shelters or changing activity levels can also help maintain body temperatures. Body shapes (surface to volume ratio), body colour, and the properties of body fat and skin can all affect heat retention, absorbance and loss.

Smaller species may have less scope for accessing these alternative solutions. This is because their smaller size may place restrictions on their adoption; including both physical restrictions (fur thickness is limited by body size) and biological restrictions (colour change or activity changes can increase predation risk). Such factors may mean that smaller mammals are more dependent on basal heat generation as a means of maintaining a constant temperature than are larger mammals.

The research team are keen to see if the same pattern of strong Temperature – BMR relationships at smaller body mass but not at bigger body mass, hold true with birds as well.

This research was published in The American Naturalist.

Resources mediate selection on module longevity in the field

Authors: Karin Svanfeldt, Keyne Monro, and Dustin J Marshall

Published in: Evolutionary Biology

Abstract

The life histories of modular organisms are complicated, where selection and optimization can occur at both organismal and modular levels.

At a modular level, growth, reproduction and death can occur in one module, independently of others. Across modular groups, there are no formal investigations of selection on module longevity.

We used two field experiments to test whether selection acts on module longevity in a sessile marine invertebrate and whether selection varies across successional gradients and resource regimes.

We found that selection does act on module longevity and that the strength of selection varies with environmental conditions. In environments where interspecific competition is high, selection favours colonies with longer zooid (module) longevity for colonies that initially received high levels of maternal investment. In environments where food availability is high and flow rate is low, selection also favours colonies with longer zooid longevity.

These patterns of selection provide partial support for module longevity theory developed for plants. Nevertheless, that selection on module longevity is so context‐dependent suggests that variation in module longevity is likely to be maintained in this system.

Svanfeldt K, Monro K, Marshall DJ (2018) Resources mediate selection on module longevity in the field, Journal of Evolutionary Biology PDF DOI 

Sizing-up the impacts of fluctuating resources on body size

Recent work in the Centre for Geometric Biology has found that smaller algal cells had slower growth, lower storage of phosphorous and poorer recovery from phosphorous depletion but, interestingly, there was no effect of size when nitrogen was limiting.

Resource levels, such as food or nutrients, are rarely constant in nature but tend to fluctuate through time and across space. Such fluctuations in resources might have different impacts on organisms of different sizes but current ecological theories differ in their predictions of how the evolution of body size will be influenced by pulse inputs of food or nutrients.

While this is theoretically interesting, there is also a more pressing need for improving our understanding of such geometric biology. Phytoplankton cells are becoming smaller as a result of increased temperature and ocean acidification and we need to be able to better predict the consequences of this size shift under varying levels of resources.

Martino Malerba, Maria Palacios and Dustin Marshall have been able to test predictions from three different models of resource-use by using algae that have been genetically modified. They used 280 generations of artificial selection to create larger and smaller phytoplankton cells differing by as much as 1000% in mean body size.  

Cells were exposed to various resource levels by manipulating nitrogen (N) and phosphorous (P) in the growth media, to quantify how size can influence the ability of a species to cope with unpredictable nutrient conditions. 

Martino and his colleagues considered three different ecological theories that differ in their predictions on how size should mediate responses to fluctuating resources.  

  1. The ‘Fasting Endurance Hypothesis’ would predict that larger cells are more buffered against periods of nutrient limitation.
  2. The classic ‘r-K Selection Theory’ predicts that smaller cells with faster generation times will be better placed to take advantage of a nutrient pulse and so recover quickly from periods of nutrient limitation.  
  3. The ‘Metabolic Theory of Ecology’ would predict that tolerance to nutrient deprivation would decrease with increasing mass specific metabolic rate of an organism.

For the phytoplankton species used in this study (Dunaliella tertiolecta), the mass specific metabolic rate increases with size which means that larger cells should grow faster but be less tolerant to nutrient depletion than smaller cells. 

So which theory turned out to be correct?  The team found that periods of P depletion had a greater negative effect on smaller cells as predicted by the ‘Fasting Endurance Hypothesis’ but there was no effect of size on response to N depletion which was not predicted by any of the theories. 

Overall Martino, Maria and Dustin were able to determine that size interacts with stored resources in different ways. Increasing size can promote the ability to use stored P to supplement growth in D. tertiolecta, whereas the ability to store and utilise N does not change across sizes.

Transmission Electron Microscopy (TEM) photos with false coloring showing different densities of internal nutrient reserves between evolved algal cells from small-selected and large-selected lineages.
Mean population growth rate (with 95% confidence intervals) for each size-selected lineage of Dunaliella tertiolecta after experiencing nutrient-replete (red), nitrogen-deplete (green) or phosphorous-deplete conditions (blue) pre-trial conditions.

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