Journal Club

Highlighting recently published papers selected by Academy members

Seasonality shapes coevolution of parasites and hosts

Moderate seasonal swings maximize the intensity of coevolution among bacteria and bacteriophages. Image credit: Science Source/Dennis Kunkel

Moderate seasonal swings maximize the intensity of coevolution among bacteria and bacteriophages.                                               Image credit: Science Source/Dennis Kunkel

Parasites and their hosts coevolve in an arms race influenced by environmental conditions. Seasonal change, for example, can shape the course of evolution, but precisely how has been something of a mystery. A recent study used lab experiments and mathematical modeling to tease out one potentially important pattern: the intensity of this coevolution peaks when the extent of seasonal change is moderate rather than mild or extreme.

The study, published in Proceedings of the Royal Society B, showed that the bacterium Pseudomonas fluorescens and its associated bacteriophage, SBW25φ2, evolved their strongest defenses and infectivity when the host and parasite grew together in media with moderately fluctuating nutritional values, representing seasonality over time. While coevolution is a classic topic in ecology, the effect of seasonal environmental variation is less well understood and rarely experimentally tested, notes coauthor Charlotte Ferris, who led the study as a mathematics PhD student at the University of Sheffield in the United Kingdom.

Ferris had previously published a 2018 theoretical study that used a classic epidemiological model to predict the progress of an infection through a host community. That model assumed that only the host evolved, but not the parasite. Variables including host population size, birth rates, death rates, and infection and recovery rates were factored into the model. The earlier study assumed that host birth rates would fluctuate due to the environment, but that they would do so symmetrically around a mean value, such that average birth rate would stay the same. The model predicted that seasonally stable environments would produce the most disease-resistant hosts.

This latest study adapted the earlier model to account for both host and parasite coevolution and experimentally tested those predictions in the lab. Again, the model assumed that average host birth rates would remain constant and predicted that stable environments would produce the most infectious phages and the most disease-resistant bacteria.

However, when Ferris tested these predictions in the lab, she found surprising results. First, she grew phage and bacteria together, allowing them to coevolve for several days in one kind of media. Then she transferred the pair into a nutritionally different media for another few days. Each pair underwent 24 such transfers between different media types. Some pairs always experienced nutritionally similar environments, mimicking mild seasonal change, while other pairs oscillated between very different nutritional environments. Control pairs experienced the same kind of media every time.

At the end of the transfer phase, bacteria from each pair were isolated and challenged to compete with phage from another pair. For example, Ferris pitted bacteria evolved in stable nutritional conditions against phage evolved in highly variable environments. She then assessed the level of resistance the bacteria had evolved and the level of infectivity the phage had evolved. Contrary to expectations, the phages that most effectively killed bacteria, and the bacteria that most effectively fought off phage, were those that had coevolved in moderately variable environments rather than in stable ones.

To understand why, Ferris turned back to her model and the initial assumption that average bacterial birth rates are constant even in variable environments. The experiments suggested otherwise. When Ferris updated her models to account for variable average birth rates, her predictions were much more similar to her experimental results.

Evolutionary ecologist Pedro Vale, a lecturer at the University of Edinburgh, Scotland, who was not involved in the study, praises the work’s combination of modeling and experimentation. “Even though coevolution is an intuitive idea, it’s incredibly difficult to show empirically,” he says. And it’s even more difficult, he adds, to show that it’s influenced by the added layer of environmental variation over time. The biggest contribution of this work, he says, is concretely demonstrating that environmental fluctuation does in fact change host–parasite coevolution.

Future studies could look beyond seasonal variation to study how other kinds of environmental variation also shape coevolution, notes coauthor Alex Best, a mathematician at the University of Sheffield and Ferris’ doctoral advisor. For example, many environments are spatially heterogeneous; hosts and parasites may migrate between patches to escape or chase one another. Factoring in these migration dynamics, says Best, could improve future models.

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