Why do cooler mothers produce larger offspring?

In a recently published letter, Amanda Pettersen, Craig White, Rob Bryson-Richardson and Dustin Marshall propose a simple model to explain a pervasive conundrum – why do cooler mothers produce larger offspring?

Life history theory maintains that mothers balance the costs and benefits of making a few larger and better performing offspring against making many smaller and poorer performing offspring.

A major challenge to the theory is the fact that temperature seems to alter the optimisation of this trade off. Observations indicate that across a wide range of taxa and systems, mothers in warmer conditions produce smaller offspring. What is more, experimental studies have also shown that increasing temperatures decrease offspring size.

Amanda and her PhD supervisors are proposing that linking life history theory and metabolic theory, which relates to energy use, can provide a widely applicable explanation to the offspring size / temperature relationship.

Their model is centred on the cost of development. Mothers must provision their offspring until they are able to feed for themselves, that is, attain nutritional independence. The time spent in this developmental phase coupled with the energy expended will comprise the ‘cost’ of development. The minimum offspring size that allows individuals to reach nutritional independence must, then, increase with increasing cost of development.

As temperatures increase, developmental rate is expected to increase so that less time is spent in the developmental phase and metabolic rates (rates of energy use) are also expected to increase. The research team are suggesting that we consider how sensitive these two components are to temperature. If developmental rate is more sensitive to changes in temperature than metabolic rate, then the cost associated with provisioning offspring to achieve nutritional independence will decrease with increasing temperatures.

Or to put it another way, if developmental rate increases more than metabolic rate as temperatures rise, so that the developmental time is shorter in relation to metabolic rate, then the developmental cost is lower and offspring are smaller at higher temperatures. If, however, metabolic rate is more sensitive to changing temperatures than developmental rate then the converse is true; the developmental cost will increase with increasing temperatures and offspring are predicted to be larger at higher temperatures.

In order to develop and test these ideas the team needed to generate measures of temperature dependence of metabolic rate and developmental rate simultaneously, something that hadn’t been done before in a systematic fashion.

They started by methodically searching published literature to determine the relationship between the temperature that mothers experience and the size of their offspring. They then experimentally manipulated temperature to examine how developmental rate and metabolic rates changed in two very different species – the bryozoan Bugula neritinaand the zebrafish Danio rerio. They used the data from these experiments to develop the mathematical functions for their model to determine how the costs of development change with temperature. Finally they searched the literature again to get data on the temperature dependence of developmental and metabolic rates for a wide range of species because they wanted to test whether their model could apply more generally.

Amanda and her colleagues found that the offspring size / temperature relationship is widespread. Also in the two species they collected experimental data for, they found that development time is more sensitive to temperature than metabolic rates. This means that the overall costs of development decrease with temperature. What is more, they found that this pattern applies more broadly – for 72 species across five phyla the costs of development are higher at cooler temperatures.

Combining life history theory and metabolic theory has allowed the research team to provide a general explanation for offspring size / temperature relationships. In colder temperatures mothers show an adaptive response whereby they offset the increased costs of development by making larger offspring that possess greater energy reserves.

This research is published in the journal Ecology Letters.

This figure shows the relationship between two biological rates; development time (D) and metabolic rate (MR). In the left-hand graph we can see that as temperature increases from T4 to T1, development time is expected to decrease and metabolic rate is expected to increase. The right-hand panels demonstrate what is predicted to happen when b) the developmental rate is more sensitive to temperature than metabolic rate and so c) the total costs of development (and therefore offspring size) should decrease with increasing temperature. In d) the converse is true – metabolic rate is more sensitive to temperature than developmental rate and so e) total costs of development (and offspring size) will increase with increasing temperature.

New projects 2019

A number of large new projects will be getting underway in 2019 as a result of ARC funding schemes. Dustin Marshall and Matt Hall are now Future Fellows and Giulia Ghedini has received a Discovery Early Career Researcher Award. Dustin and Giulia will be using marine invertebrates to look into impacts of global warming whilst Matt is tackling the importance of sex in the evolution of infectious disease.

Within a given species, often the greatest heterogeneity that a pathogen will encounter will be due to differences between males and females. Yet, up until recently, insight into this crucial topic was driven by research into one sex, typically males.


Matt’s recent work has shown that, in the water-flea Daphnia magna, not only is pathogen fitness lower in males, but so is a pathogen’s evolutionary potential. What is more, the relative proportion of males in a population can fundamentally alter the overall transmission potential of a pathogen.

A. The graph on the left demonstrates that pathogen fitness is sex specific; in this case pathogen fitness is greater in females. B. The graph on the right indicates how changes in the relative proportion of males can increase the burden of disease for every individual.

This project was stimulated by Matt’s recognition that there is an absence of theory that explicitly considers how males and females can impact on the evolution and epidemiology of infectious disease.  Matt is seeking to address this imbalance and integrate sex-specific effects into a general framework for disease evolution and epidemiology.

Matt will be using the water-flea Daphnia magnaand its associated pathogens to provide an experimental system in which he can manipulate infections in males and females, characterise the degree of differentiation, and generate predictive models.


Dustin will be investigating how temperature affects the life-history stages of feeding and non-feeding larvae. Marine life histories show strong biogeographic patterns: warmer waters favour species with feeding larvae and cooler waters favour species with non-feeding larvae. Warming could be particularly problematic for Australian species because in 2012, Dustin discovered that Australian coastal species predominantly have non-feeding larvae. This means that future temperatures increases could affect native Australian invertebrates disproportionately relative to other regions of the world. (Put in schematic from application here)

Schematic of the data pipeline to estimate developmental energetics across temperature regimes. For each species, parents will be exposed to a range of temperatures, after which the size and number of offspring that are produced will be measured. These offspring will then have every phase of their energy usage and acquisition, from fertilisation through to metamorphosis estimated across an orthogonal temperature range. Dustin will then integrate these estimates to create a thermal energy performance curve for each species and use these data to parameterise models of connectivity, viability and life history evolution.

At the end of an intensive experimental period, Dustin will have quantitative estimates of how temperature alters the success of a range of species from the gamete to the juvenile. At this stage Dustin will work with collaborators to generate predictive models to determine

  1. how does temperature alter the relative advantages for each of the two developmental modes?
  2. how does temperature affect dispersal and connectivity among populations for each developmental mode? and finally
  3. how does temperature affect the distribution of marine organisms with feeding or non-feeding larvae?


Giulia will be investigating how global warming will affect entire ecological communities.

We already know that warming can affect individuals by reducing their body size and speeding up energy use, as well as reducing water viscosity.  But what we don’t know is how these changes at the individual level might play out at the population and community level and affect the energy intake or expenditure of whole communities.

Giulia will be looking at how changes in body size at the individual level interact with population and community level ecosystem functions.

Giulia is particularly interested in this knowledge gap and will be investigating the implications of warming sea temperatures for important ecosystem functions such as productivity, food web stability or resistance to invasion.

Giulia has planned a series of experiments, using communities of easily manipulated, sessile, marine invertebrates, to explore 4 main questions.

  1. How do changes in community size-structure and composition under warming alter the energy intake (phytoplankton) and expenditure (oxygen) of marine invertebrate communities?
  2. Since the availability of energy can mediate biological invasions, does warming alter the energy usage of communities so that they are more susceptible to invasive species?
  3. Are the responses of invertebrate communities to warming mediated by changes in their food (phytoplankton)?
  4. Given that warming reduces water viscosity, how does this mechanical effect alter food consumption and metabolic expenditure in marine communities of different size-structure?

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


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


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