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

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 

Do larger individuals cope with resource fluctuations better? An artificial selection approach

Authors: Martino E Malerba, Maria M Palacios, and Dustin J Marshall

Published in: Proceedings of the Royal Society B

Abstract

Size determines the rate at which organisms acquire and use resources but it is unclear what size should be favoured under unpredictable resource regimes.

Some theories claim smaller organisms can grow faster following a resource pulse, whereas others argue larger species can accumulate more resources and maintain growth for longer periods between resource pulses. Testing these theories has relied on interspecific comparisons, which tend to confound body size with other life-history traits.

As a more direct approach, we used 280 generations of artificial selection to evolve a 10-fold difference in mean body size between small- and large-selected phytoplankton lineages of Dunaliella tertiolecta, while controlling for biotic and abiotic variables. We then quantified how body size affected the ability of this species to grow at nutrient-replete conditions and following periods of nitrogen or phosphorous deprivation.

Overall, smaller cells showed slower growth, lower storage capacity and poorer recovery from phosphorous depletion, as predicted by the ‘fasting endurance hypothesis’. However, recovery from nitrogen limitation was independent of size—a finding unanticipated by current theories.

Phytoplankton species are responsible for much of the global carbon fixation and projected trends of cell size decline could reduce primary productivity by lowering the ability of a cell to store resources.

Malerba ME, Palacios MM, Marshall DJ (2018) Do larger individuals cope with resource fluctuations better? An artificial selection approach, Proceedings of the Royal Society B, PDF DOI 

On the interplay among ambient temperature, basal metabolic rate, and body mass

Authors: Daniel E Naya, Hugo Naya, and Craig R White

Published in: The American Naturalist

Abstract

One of the most generalised conclusions arising from studies analyzing the ecological variation of energy metabolism in endotherms is the apparent negative correlation between ambient temperature and mass-independent basal metabolic rate (residual BMR). As a consequence, ambient temperature has been considered the most important external factor driving the evolution of residual BMR.

It is not clear, however, whether this relationship is size dependent, and artifacts such as the biased sampling of body masses in physiological data sets could cause us to overstate the ubiquity of the relationship.

Accordingly, here we used published data on body mass (mb), BMR, and annual mean temperature (Tmean) for 458 mammal species (and/or subspecies) to examine the size dependence of the relationship between temperature and BMR.

We found a significant interaction between mb and Tmean as predictors of residual BMR, such that the effect of Tmean on residual BMR decreases as a function of mb. In line with this, the amount of residual variance in BMR explained by Tmean decreased with increasing mb, from 20%–30% at body sizes of less than 100 g to almost 0 at body sizes greater than 1,000 g.

These data suggest that our current understanding of the importance of broad-scale variation in ambient temperature as a driver of metabolic evolution in endotherms probably is affected by the large number of small species in both nature and physiological data sets.

Naya DE, Naya H, White CR (2018) On the interplay among ambient temperature, basal metabolic rate, and body mass. The American Naturalist, PDF DOI 

Causes and consequences of variation in offspring size

Offspring size affects all aspects of an organism’s life, from birth through to reproduction, and  studies show that larger offspring do better overall. 

Despite the long standing interest in the drivers of differences in offspring size, most studies focus only on one particular taxon or system.

Dustin Marshall, Amanda Pettersen and Hayley Cameron were interested in looking at offspring size across all taxa and at different levels of organisation – within a brood, between individuals and across different species and environments – to see if this wider scope could help them better understand the causes and consequences of variation in offspring size.

They started by looking at a pattern that will be familiar to many ecologists and bio-geographers; offspring size tends to get bigger as you move from the tropics to the poles. They found that this was true for practically all species they compiled data for, with the notable exception of turtles and plants. 

Dustin, Amanda and Hayley suspect that the difference in the patterns they recorded relates to the way offspring size and temperature affects development.  Small increases in temperature are known to yield large increases in development rate. The lower number of warmer days in higher latitudes might just mean that there just isn’t time for larger seeds or turtle eggs to complete development. Importantly, turtles don’t incubate their eggs and so will be more susceptible to environmental temperature than taxa that do (birds for example). Collecting data on egg size variation in other reptiles would help to test this theory.  

For taxa such as fish, amphibians and invertebrates the overall smaller egg size in comparison to seeds and other vertebrates might preclude development time as a limitation on size.

Offspring size also varies across populations and within broods from the same females.  Dustin and colleagues highlight that sources of variation might be external whereby mothers buffer their offspring from harsher environments by making them bigger, or choose to maximise numbers in more benign environments, meaning that offspring are smaller. Mothers might also provision offspring unequally within a brood to ensure that whatever environment the offspring find themselves in, some at least, will do well.  

Hayley’s PhD work however, suggests that variation in size within a brood reduces competition between siblings and all offspring, regardless of their size, do better.

Finally the team considered the question as to why larger offspring generally tend to perform better than smaller offspring. They were interested in understanding the costs and benefits of a larger size to the energy available for fitness-enhancing functions such as growth and reproduction.  

It seems that larger offspring often access more energy resources than smaller offspring. In plants, seed size likely affects photosynthetic capacity, in certain fish and snakes, a larger gape size at birth allows for more efficient energy acquisition and, in filter feeding invertebrates, larger offspring initially produce more or larger feeding structures. In addition, larger offspring should expend relatively less energy than smaller offspring and complete energetically costly developmental stages with more energy reserves intact.

This research was published in the journal Functional Ecology.