Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes

Authors: Tim Connallon, Shefali Sharma, and Colin Olito

Published in: The American Naturalist

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes.

Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time.

This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of “sexually antagonistic” alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions.

We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation.

We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity.

The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

Connallon T, Sharma S, Olito C (2018) Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes, The American Naturalist PDF DOI

Growing pains: time to reassess models of growth?

A central aim of the Centre for Geometric Biology is understanding how and why organisms grow. In a recent opinion piece, published in the journal Trends in Ecology & Evolution, Dustin Marshall and Craig White suggest that it might be time to take another look at the ways we currently understand and model growth.

In the past, growth has mainly been considered in two different ways. Mechanistic models of growth emphasise identifying the physiological processes driving growth. This group of models includes the von Bertalanffy Growth Function, which is perhaps the best-known growth model. It estimates the rate of increase in mass (growth) as the difference between anabolism (energy-consuming processes) and catabolism (energy-producing processes). Other models of this type include the Ontogenetic Growth Model and the Dynamic Energy Budget model.

In contrast, phenomenological models of growth are based on life-history theory and work from the assumption that organisms evolve to maximise their fitness. Theories and models under this framework revolve around the trade-offs between maximising reproduction against the risk of mortality.

The von Bertalanffy Growth Function and more recent mechanistic models do an excellent job of describing how the growth of most organisms slows as they approach their final size. Models such as these assume that growth slows or stops because the organism cannot acquire, distribute or use resources faster than it has to expend them on self-maintenance.

There is a problem however. Mechanistic models do not adequately consider reproduction — an energetically expensive undertaking. Most mechanistic models make the simple but crucial assumption that reproduction is proportional to body size, and that allocation to reproduction begins at birth and remains a constant fraction of total body size throughout an individual’s life. While this assumption seems unrealistic, it is essential for these models to describe growth well.

Phenomenological models tend to have different dynamics for juvenile and mature phases; after maturity, increasing allocation of resources to reproduction reduces growth. But again, most of these models assume that reproductive output is directly proportional to body size.

We now know that, for marine fish at least, reproductive output is disproportionally higher in bigger females. Dustin and Craig suspect that this pattern is the rule for most taxa but that it has been overlooked (see Figure 1).  If this does occur more generally, what does it mean for our understanding of growth?

Figure 1. Data from a range of taxa (A = marine invertebrates and B = other taxa) showing the disproportionate increase in reproductive output at larger sizes. The dotted line in each case shows what a 1:1 (or isometric) scaling of reproduction with growth would look like.

Dustin and Craig argue that many of the mechanistic models of growth are trying to explain dynamics that are driven by increasing allocation to reproduction but they do not allow for it.  Instead, these models assume that resource supply decreases as individuals get bigger so that if the allocation to reproduction is allowed to increase then organisms will shrink once they start to reproduce.

A common feature of both theoretical approaches is that they assume that the relative amount of energy available for total production decreases with size.  If we instead assume that resource acquisition and usage both change in the same proportions in relation to size, and combine those parameters with the disproportionate increase in reproductive output (hyperallometry), then we can predict growth trajectories remarkably well (see Figure 2).

Dustin and Craig posit that the growth dynamics that biologists have long sought to understand emerge simply from hyperallometric scaling of reproduction.

Figure 2. Dustin and Craig propose a simple model that allows energy intake and expenditure to scale consistently with size, but reproductive output to increase disproportionately with size. To illustrate that this “hyperallometric reproduction” model describes growth patterns on par with well-known mechanistic models, Dustin and Craig have used data for cod Gadus morhua and have fitted model outputs for the van Bertanalaffy Growth Function (orange), the Ontogentic Growth Model (blue) and the hyperallometric reproduction model shown in red.

 

Research fellow position: marine larval biologist

  • Level A, research-only academic
  • $66,706 to $90,532pa + 9.5% superannuation
  • Full-time, starting late 2018
  • Two-year, fixed-term
  • Monash University Clayton campus

Professor Dustin Marshall is seeking a marine larval biologist, with strong quantitative skills, to explore the ways in which temperature affects the energetics of development in marine invertebrates.  This position will be with the Centre for Geometric Biology within the School of Biological Sciences at Monash University.

As the successful candidate, you will be expected to undertake experiments to determine the relative performance of different larval types across every stage of the life history, but more importantly demonstrate a strong conceptual understanding of relevant life history theory and have a demonstrated track record in producing high quality publications.

Key selection criteria

  1. A doctoral qualification in larval biology
  2. Demonstrated analytical and manuscript preparation skills; including an excellent track record of refereed research publications in high impact journals
  3. Demonstrated experience in empirical research using cutting-edge quantitative approaches
  4. Ability to solve complex problems by using discretion, innovation and the exercise of diagnostic skills and/or expertise
  5. Well-developed planning and organisational skills, with the ability to prioritise multiple tasks and set and meet deadlines
  6. Excellent written communication and verbal communication skills with proven ability to produce clear, succinct reports and documents
  7. A demonstrated awareness of the principles of confidentiality, privacy and information handling
  8. A demonstrated capacity to work in a collegiate manner with other staff in the workplace
  9. Demonstrated computer literacy and proficiency in the production of high level work using software such as Microsoft Office applications and specified University software programs, with the capability and willingness to learn new packages as appropriate.

Enquiries to Professor Dustin Marshall on +61 3 9902 4449

For more information, or to apply, refer to the Monash University website

Have we outgrown the existing models of growth?

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Theories of growth have a long history in biology. Two major branches of theory (mechanistic and phenomenological) describe the dynamics of growth and explain variation in the size of organisms. Both theory branches usually assume that reproductive output scales proportionately with body size, in other words that reproductive output is isometric.

A meta-analysis of hundreds of marine fishes contradicts this assumption, larger mothers reproduce disproportion- ately more in 95% of species studied, and patterns in other taxa suggest that reproductive hyperallometry is widespread.

We argue here that reproductive hyperallometry represents a profound challenge to mechanistic theories of growth in particular, and that they should be revised accordingly. We suspect that hyperallometric reproduction drives growth trajectories in ways that are largely unanticipated by current theories.

Marshall DJ, White CR (2018) Have we outgrown the existing models of growth? Trends in Ecology & Evolution PDF DOI

Parental environment influences the adaptive potential to global change

A new study indicates that parental environment can influence adaptation to projected increases in sea level temperatures, not only by altering the fitness of offspring but also by altering the genetic variance available to increase fitness.

Evatt Chirgwin, along with his PhD supervisors Dustin Marshall, Carla Sgro and Keyne Monro, were interested in how, in the face of global change, populations can maintain or recover fitness. Evatt used a small, marine tubeworm Galeolaria caespitosa to examine how parental exposure to projected ocean warming affects adaptive potential for survival during the most vulnerable early life stage.

Individuals faced with environmental stress can respond through ‘plastic’ changes to morphology, physiology and/or behaviour and these changes can persist in their offspring. But in order for populations to persist in the longer term, they will often require adaptive evolution, which rests on the availability of adequate genetic variation.

Galeolaria is an external fertiliser which allowed Evatt to manipulate fertilisation across different males and females as well as exposing parents and embryos to different temperatures. Evatt took sperm from each male parent and crossed it with eggs from multiple females and vice versa; a design that allowed him to estimate genetic variance and therefore adaptive potential to ocean warming.

Embryos and larvae are the life stages most sensitive to stress in marine invertebrates, and are key to assessing vulnerability to ocean warming. Evatt measured survival of 20,000 Galeolaria offspring as a measure of fitness where parents were exposed to two temperatures prior to spawning and offspring were then reared in the same two temperatures.

The team found that mean offspring survival was higher when offspring were reared at the same temperatures as their parents, but also that parental exposure to warming altered genetic variance.  This means that parental environments may have broader ranging effects on adaptive capacity to global warming than is currently appreciated. 

While effects were subtle, even this modest buffering may help natural populations to persist under rising ocean temperatures. This study is an important step towards understanding how plasticity and adaptation jointly shape population dynamics and extinction risks under global change.

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

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.