Linking life-history theory and metabolic theory explains the offspring size-temperature relationship

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson‐Richardson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved.

We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla.

We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters PDF DOI

Why release small amounts of sperm slowly?

Sperm competition theory has been central to our understanding of male reproductive biology for many years and is dominated by the idea that males compete strongly to fertilise female’s eggs. But in many species the external environment will also influence reproductive strategies and, in their new publication, Colin Olito and Dustin Marshall ask an obvious but neglected question “what would reproductive strategies look like in the absence of sperm competition?”

Their interest was sparked by the fact that broadcast spawning species (e.g. seaweeds, corals annelid worms, sea stars and many fish taxa) release sperm and eggs to be fertilised externally, which provides an increased opportunity for the environment to influence the evolution of spawning strategies when compared to internal fertilisers.

In addition, broadcast spawners also have spawning strategies that differ markedly from predictions arising from classic sperm competition theory. For example, many broadcast spawning species have very long spawning times characterised by slow individual gamete release rates and, what is more, large males do not necessarily release more sperm than small males despite a large investment in gonads; neither strategy is predicted by classic theory.

Colin and Dustin devised two experiments to consider how fertilisation success changes with the amount of sperm released (ejaculate size) and the rate at which it is released. They used a marine intertidal polychaete worm, Galeolaria caespitosa, that has separate sexes and releases gametes initially into its tube and then, through rhythmic whole-body contractions, out of the tube in slow steady pulses.

A female Galeolaria removed from its tube and releasing eggs.

By repeatedly injecting different volumes of sperm (at the same concentration) and at different speeds into a flume set up to have laminar flow, Colin and Dustin were able to measure the fertilisation success of eggs placed ‘downstream’ of the sperm injection point.

Experimental set-up using the flume. Laminar flow was achieved by using collinators (drinking straws).

They used an experimental design that ensured that there was no variation in the number of males contributing to the pooled ejaculate used for the different experimental treatments. So, strictly speaking the experiments were not done in the absence of sperm competition, but, instead, in the absence of variation in sperm competition.

Colin and Dustin found that the benefits of releasing sperm quickly or slowly depended on ejaculate size: when only a small amount of sperm was released, it was better to release it slowly but when ejaculate size was larger and released at a faster rate, fertilisation success was greater for eggs further away. However, there was a substantial ‘cost’ associated with this higher fertilisation success for distant eggs. The more sperm males release, the more is wasted during sperm dispersal.

Colin and Dustin’s study suggests that slow sperm release rates are expected to evolve whether or not males experience strong sperm competition, and highlight the importance of taking account of selection from the external environment when seeking adaptive explanations for male broadcast spawning strategies.

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

The evolution of males and females depends on the environment

Opportunities for adaptation in females and males are mediated by life history and population characteristics that vary widely between species. Combining these factors with environmental heterogeneity can yield surprising evolutionary outcomes that are not always predicted by classic theories that deal with each factor separately.

Tim Connallon, Shefali Sharma and Colin Olito have analysed four simple models of evolution of female and male adaptations in changing environments. They compared the outcomes to classical population genetics models of sex-specific selection in stable environments and found some important differences.

Females and males make roughly equal genetic contributions to offspring. Consequently, the response to natural selection tends to depend equally on the pattern of selection in each sex. Selection does not necessarily increase adaptation of both sexes, but instead favours evolutionary changes in which the gains in adaptation for one sex are sufficient to offset any reductions in adaptation for the other. Such ‘sexually antagonistic’ selection is common and contributes to the maintenance of genetic variation.

Classical population genetics theory predicts that, where there are separate sexes, natural selection will favour genotypes that allow fitness across both males and females to be maximised. While these theories have proved extremely useful they tend to focus on evolution in constant environments – a condition that will be violated in many species.

Tim and his colleagues are interested in the outcomes of sex-specific selection in variable environments and how the life history and demography of a species’ can influence evolutionary dynamics. To this end they developed four mathematical models that vary in the life stage, or the sex, that disperses through a spatially or temporally heterogeneous environment.

In the first model, adults of both sexes disperse from the areas they were born in, with local selection happening before dispersal, and mating and reproduction happening after dispersal. This scenario applies to species with relatively immobile early-life stages, including many vertebrate and insect taxa. The second model considers taxa that have highly mobile early life-stages such as seed dispersal in plants or larval dispersal in many aquatic organisms. In the third example, adults from only one sex disperse from the area they were born in, prior to mating and reproduction. Sex biased migration is common in animals and can be strongly female biased or male biased. Finally, the fourth model deals with sex-specific selection that changes over time but is uniform across space.

When they ran these four different models and compared the outcomes with predictions from the classical population genetics models, they found the details of a species’ life history and demography were critical to determining the evolutionary dynamics of sex-specific adaptations.

For example, the models predict that conspicuous sex-limited colour polymorphisms (the simultaneous occurrence of multiple phenotypes limited to one sex only) should be particularly common in species that have strong sex-biased migration (scenario 3) and species where dispersal occurs early in the life cycle (scenario 2).

This work paves the way for diversifying the range of species that serve as models for studying sex-specific adaptations.

This work has been published in The American Naturalist.

Model outputs demonstrating that environmental variability promotes the maintenance of genetic variation beyond the comparatively restrictive conditions for polymorphism in a constant environment (solid grey versus dotted grey curves). Solid pink and blue lines indicate the likelihood of a beneficial allele becoming fixed for males and females in the different scenarios and over increasing selection pressure. Note that the pink curves overlay the blue curves in Models 1 and 4 and in Model 3 the equivalent results (with sexes reversed) would be obtained if there was female-limited dispersal.

Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

Authors: Colin Olito and Dustin J Marshall

Published in: Journal of Evolutionary Biology

Abstract

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory – broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal.

Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae).

We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size.

Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

Olito C, Marshall DJ (2018) Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae), Journal of Evolutionary Biology PDF DOI 

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