Dustin Marshall: Mother-offspring conflicts: Temperature can change selection on offspring size

Professor Dustin Marshall, Australian Research Council Fellow and the Head of the Marine Evolutionary Ecology Research Group / Centre for Geometric Biology at Monash University, discusses with us his recently accepted paper “Temperature-mediated variation in selection on offspring size: a multi-cohort field study.”

What is the background to your paper?

We know offspring size varies enormously and understanding this variation is a long-standing goal of life history theoreticians and ecologists alike. A particularly interesting facet of offspring size is the fact it affects the fitness of both mothers and offspring simultaneously, so selection acts on both. This can lead to conflict over the amount of provisioning mothers provide to offspring. Selection on offspring usually favours bigger sizes, but mothers should only produce larger offspring where there is a marked benefit in performance for these offspring – there is a cost associated with this extra provisioning.

Bugula neritina with feeding tentacles. Photo credit Amy Hall

Temperature has a fairly reliable relationship with offspring size – higher temperatures are associated with smaller offspring. But what happens next? Does the relationship between offspring size and adult performance change with temperature? 

There are few studies exploring these relationships in the field because it is an onerous undertaking. Repeated estimates of selection across multiple seasons and years are required to determine whether the relationship between offspring size and adult performance varies with natural temperature fluctuations.

What is your paper about?

Bugula are settled on small plates before being deployed in the field

This study aims to fill that gap. Using the model marine invertebrate species Bugula neritina, I deployed over 6000 individuals of known offspring size into the field over a period of 4 years. In total I had 28 cohorts, each of approximately 240 individuals, where I measured survival, growth and reproduction of all individuals and also accessed water temperature data for the entire period.

Research assistant Annie Guillaume monitors growth and survival of Bugula in the field

Using the data I collected in this study I ran a simple ‘optimisation’ model which predicts cooler temperatures favour mothers producing larger offspring, while higher temperatures favour mothers producing smaller offspring.  And, this works the other way around too. Larger offspring are favoured at cooler temperatures, smaller offspring are favoured at higher temperatures. In other words, at higher and lower temperatures, selection pressures on both mothers and offspring are the same; their interests are aligned.

Were you surprised by anything when working on it?

There was a catch.  At intermediate temperatures a conflict emerged. From around 18-22°C it is still better to be larger from the offspring’s perspective. Larger offspring had higher survival and growth than smaller offspring but the benefits were not enough to offset the costs to the mother of producing larger offspring. At these temperatures, mothers are better served by producing smaller offspring.  This means at intermediate temperatures we would predict different offspring sizes to be favoured, depending on which perspective is taken.

Snorkellers at the field site. Panels with plates attached hang upside down in the marina

I also estimated the temporal autocorrelation of selection on offspring size among cohorts. In other words, knowing the selection coefficient on offspring size of one cohort, can we predict the selection coefficient of the next? Surprisingly, the answer was yes. But maybe even more surprising was that selection during one cohort was negatively correlated with selection two cohorts from now. So, it seems that selection varies from one generation to the next but this variation is not entirely random.

Where would you like to do next?

Newly settled Bugula on experimental plate.

Estimating temporal autocorrelation is a notoriously data-hungry exercise which is exacerbated here because I am interested in selection in each cohort. This means I only have selection estimates for 28 cohorts despite the scope of the study. I plan to resume estimating selection on offspring size to see whether these patterns persist, as soon as Covid-19 obstacles are removed. 

At the same time, I will see whether the relationships between offspring size, adult performance and temperature, change when offspring settle within a community. Does the presence of other species tip the balance in selection on offspring size?

Did you have any problems setting up the experiment?

To do this experiment I collected adult colonies of Bugula and spawned them in the lab, before putting the newly settled Bugula back out in the field. Unfortunately, I had to use different sites for collection of adult Bugula and field deployment of newly settled colonies. This was not ideal. The brood stock collection site has reproductive colonies all year round but experimental colonies deployed there suffer mass die off in late summer.  In contrast, our field deployment site has few reproductive colonies at certain times of year but colonies survive the high summer temperatures much better. Luckily temperature regimes between the two sites are very similar and show the same trends.  So, while imperfect, using two sites enabled me to conduct this experiment year-round. 

Read the article in full here.

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