Dr Alex Strauss  is a Postdoctoral Research Assistant at the University of Minnesota and winner of the 2018 Haldane Prize for Early Career Researchers for his paper, Linking host traits, interactions with competitors and disease: Mechanistic foundations for disease dilution.

In this Insight, he talks about the background behind his paper, digs into disease, dilution and biodiversity, and what he wants to see happen next in this area.

What is the background behind your paper?

I focused my dissertation on studying the relationship between biodiversity and disease. I was (and still am) enthralled with the prospect of ‘dilution effects’. Dilution effects occur when a focal species experiences lower disease risk in more diverse communities. Thus, dilution effects seem like tantalizing win-wins for conservation (goal of maintaining biodiversity) and disease control (goal of managing disease outbreaks). What a cool idea! In practice, dilution effects are inconsistently observed because… well, community ecology is complicated. Of course, “diversity” (defined in various ways) can influence “disease” (defined in various ways) in a lot of different ways. Diversity can ‘dilute disease,’ ‘amplify disease,’ or have no effect on disease at all, for a variety of reasons. Dilution effect research has become quite controversial, and I would argue that a lot of the controversy stems from this complexity. Critics question its generality (how often does diversity actually reduce disease?) and argue that dilution effects are too simplistic and idealistic to be predictive or useful. The tone of the debate has become increasingly argumentative and perhaps counterproductive (Halsey 2019).

As a graduate student reading broadly, it struck me that critiques and syntheses about diversity-disease relationships were plentiful, but experiments that actually delineated when, why, and how diversity might shape disease seemed relatively rare. Two of the most influential papers for me early in graduate school were Keesing et al. (2006) and Johnson and Thieltges (2010). These papers clearly outline ways that ‘diluter’ taxa could inhibit disease transmission. Still, when I surveyed the literature, very few experiments grappled with these mechanistic species interactions among focal hosts, ‘diluter’ taxa, and parasites. Without such clear foundations, dilution effect research seemed doomed to remain controversial. Wouldn’t it be more satisfying to delineate when and why diversity reduced disease, rather than argue about how frequently dilution effects arise? So the goal of my dissertation, and the motivation behind this paper, was to experimentally test stronger mechanistic foundations for general dilution theory.

How did you come up with the idea for your paper?

The zooplankton study system that I worked on as a graduate student turned out to be ideally suited for testing mechanistic dilution theory, for two reasons. First, we already knew that lakes with higher zooplankton diversity had smaller fungal epidemics (parasite: Metschnikowia bicuspidata) in populations of our focal host, Daphnia dentifera. So ultimately, this paper was inspired by a pattern that my advisor Spencer Hall had previously observed in nature (Hall et al. 2009, Hall et al. 2010). Moreover, I discovered that this pattern of disease dilution was driven by one key ‘diluter’ taxon, Ceriodaphnia sp., that was especially abundant in lakes with higher diversity and smaller epidemics (Strauss et al. 2016). Thus, interactions between our Daphnia focal hosts, the Metschnikowia parasite, and these Ceriodaphnia diluters seemed highly relevant for understanding the dilution effect patterns that we had observed in the field.

Second, Daphnia reproduce asexually, and genotypes can vary in important traits such as competitive ability and susceptibility. Moreover, we could easily rear monocultures of different genotypes that varied in these traits. When my colleagues and I had previously paired Ceriodaphnia diluters with three different genotypes of Daphnia, we found that dilution effects could ‘succeed’ (i.e., lower disease with diluters), fail, or become irrelevant (Strauss et al. 2015). Thus, these two general traits of hosts – their ability to compete against conspecifics and susceptibility to infection – seemed to govern whether diluters reduced disease or not. So, this system offered a unique opportunity to test how variation and covariation in these key traits regulated interactions between focal host, parasite, and diluters.

Since we knew that interactions between our focal hosts and these key diluters drove dilution effects in nature, and that these interactions differed among host genotypes that varied in key traits, we wanted to ask how disease outcomes varied along continuous gradients of competitive ability and susceptibility. For this paper in Functional Ecology (Strauss et al. 2018), we selected 8 genotypes of focal hosts to create the gradients, grew each one with and without the key diluter in a multigenerational mesocosm experiment, and asked how variation and covariation in their traits shaped disease. I’m absolutely thrilled that this work was selected for the Haldane prize!

How is your paper different from other work in this area?

Two core results of this paper add unique contributions to the diversity-disease literature. First, we found that both host traits – competitive ability and susceptibility – governed the size of epidemics in communities with diluters. When focal hosts were stronger competitors, they suffered larger epidemics because they outcompeted diluters. In other words, when diluters were outcompeted, they were too rare to influence disease. Meanwhile, we also found that focal hosts that were more susceptible suffered larger epidemics… even when diluters were present. Thus, genetic variation in focal hosts could be as or even more important than biodiversity for shaping disease. These results may seem obvious in hindsight, but quantitative relationships between traits and the size of epidemics are essential building blocks for any general, mechanistic dilution theory. These insights were only possible because we measured host traits and created continuous experimental gradients of both competitive ability and susceptibility. Other diversity-disease experiments have quantified important traits like susceptibility, but we are unaware of other experiments that delineate disease outcomes across continuous trait gradients.

Our second core result was that diluters indirectly reduced disease by regulating the population of focal hosts, rather than by directly interfering with parasite transmission. Diluters in this zooplankton study system might have influenced disease indirectly via competition with focal hosts, or directly by ‘vacuuming’ parasites from the environment. We were able to partition these two dilution mechanisms with path models. The effect of competitive host regulation was much stronger. Multi-generational experiments, like ours, remain quite rare in the diversity-disease literature. However, the importance of traits like competitive ability and impacts of competitive host regulation may only become clear across such long-term experiments. So the aspects of this paper that set it apart from other diversity-disease research are that we manipulated continuous gradients of host traits, and we let the dynamic consequences of these traits manifest across several (~6-8) generations of competition and disease transmission.

What is the broader impact of your paper?

Dilution effect theory seems to hold broad potential to help manage disease outbreaks in humans, plants, and animals. Some days, I like to imagine that insights from these zooplankton might help someone apply dilution effect theory to address real world problems. Other days, these expectations seem idealistic and ridiculous. But if there is even a small chance that dilution effects could help protect humans from zoonotic disease, conserve threatened wildlife taxa, or boost agricultural production, then doesn’t it seem worthwhile to continue studying diversity-disease relationships? I think so, and I already explained why I think this zooplankton is such a great model for tackling these questions. Overall I remain hopeful that our knowledge of this zooplankton study system might lend insight elsewhere. After all, the traits that were important from predicting the size of epidemics in the zooplankton communities are very general: susceptibility to infection and ability to compete against conspecifics. Variance and covariance in these traits seem like important building blocks for predicting how focal hosts, parasites/pathogens, and diluters might interact in other systems too. I am actively seeking collaborations that could test applications of dilution theory toward real world problems. Please let me know if you have ideas or suggestions! 

What is the next step in this field?

One of the broader results to arise from this work is that community dynamics responded sensitively to intraspecific variation (i.e., differences among pure populations of each genotype of our focal host). These strongly diverging genotypic responses lead immediately to next the question: What community dynamics would arise from genetically diverse (and perhaps more realistic) host populations? Can competition and disease drive rapid evolution in these key traits by selecting among genotypes? If so, what would such eco-evolutionary feedbacks mean for dilution effects? I have begun to address these questions (Strauss et al. 2017), but I am just scratched the surface. I hope to continue tackling these eco-evolutionary questions about competition and disease transmission in my future research.

About The Author
How did you get involved in ecology?

I was one of those kids who was always catching frogs. I guess I just never outgrew that stage. One of my favorite activities in high school was competing in Envirothon (Iowa state champs 2007!). So as an undergraduate at Washington University in St. Louis, I joined Jon Chase’s aquatic community ecology lab. My undergraduate mentor, Kevin Smith, really got me hooked with independent research in the summer after my sophomore year. Kevin and I worked on a project about amphibian chytrid fungus (Batrachochytrium dendrobatidis) in pond communities in Missouri (Strauss and Smith 2013). I was interested in the intersection of community and disease ecology from the beginning. I especially enjoyed working in the field and being part of a big collaborative team. I even enjoyed quantifying the macroinvertebrate species from the gunky pond samples. My non-science friends definitely thought I was crazy.

What is your current position?

I am currently a postdoctoral associate at the University of Minnesota. I work with Elizabeth Borer and Eric Seabloom. We are asking questions about ecological processes that shape the diversity of pathogens (barley/cereal yellow dwarf viruses) within hosts (grasses). We are also exploring consequences of vector behavior (aphids) for disease dynamics and impacts of plant pathogens on ecosystem function. It’s been exciting to add a layer of complexity by thinking about vector demography and behavior and what it means for disease. It’s also been fun to learn how to think like a plant ecologist, sample grasslands, and identify fungal pathogens in the field. Some days I definitely miss Daphnia and sampling lakes from my kayak. Both study systems have advantages and disadvantages, but together they let me ask a broader range of interesting questions. In the future, I hope to continue working on community/disease ecology questions, using both zooplankton and grasses.

What project are you most proud of?

I’m really proud of the cohesive set of articles that emerged from my dissertation. They complement one other and paint a picture of when and why diversity matters for disease. We detected a dilution effect in the field and then used experiments to delineate the impacts of key diluters on disease transmission. In the paper highlighted in this post, (Strauss et al. 2018), we asked how traits of eight different host genotypes shaped disease dynamics in communities with and without diluters. It’s a great honor to have it chosen for the Haldane prize. I am also especially proud of a complementary paper, which in many ways seems like the capstone of my graduate work. In the complementary paper, we asked how genetically diverse host populations, including all eight of the genotypes from the Functional Ecology paper combined together, evolved in response to competition and disease. If you’re curious, please check it out! (Strauss et al. 2017)

What is the best thing about being an ecologist?

I’ve had amazing mentors and coworkers throughout my career, and working with them has been a wonderful experience. I really enjoy the flexibility that comes with being an ecologist. I love the combination of field work, lab experiments, coding, reading, and writing. There is always something new, surprising, and exciting to explain about nature, and there is always a new analytical tool to learn that can help me think about it more clearly. I’m definitely finding myself spending more and more time at my computer, so these days I especially relish all of my opportunities to get back into the field.

Hall, S. R., C. R. Becker, J. L. Simonis, M. A. Duffy, A. J. Tessier, and C. E. Cáceres. 2009. Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90:791-801.

Hall, S. R., R. Smyth, C. R. Becker, M. A. Duffy, C. J. Knight, S. MacIntyre, A. J. Tessier, and C. E. Cáceres. 2010. Why are Daphnia in some lakes sicker? Disease ecology, habitat structure, and the plankton. Bioscience 60:363-375.

Halsey, S. 2019. Defuse the dilution effect debate. Nature Ecology & Evolution 3:145-146.

Johnson, P. T. J., and D. W. Thieltges. 2010. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213:961-970.

Keesing, F., R. D. Holt, and R. S. Ostfeld. 2006. Effects of species diversity on disease risk. Ecology Letters 9:485-498.

Strauss, A., and K. G. Smith. 2013. Why Does Amphibian Chytrid (Batrachochytrium dendrobatidis) Not Occur Everywhere? An Exploratory Study in Missouri Ponds. Plos One 8:e76035.

Strauss, A. T., A. M. Bowling, M. A. Duffy, C. E. Cáceres, and S. R. Hall. 2018. Linking host traits, interactions with competitors and disease: Mechanistic foundations for disease dilution. Functional Ecology 32:1271-1279.

Strauss, A. T., D. J. Civitello, C. E. Cáceres, and S. R. Hall. 2015. Success, failure and ambiguity of the dilution effect among competitors. Ecology Letters 18:916-926.

Strauss, A. T., J. L. Hite, M. S. Shocket, C. E. Cáceres, M. A. Duffy, and S. R. Hall. 2017. Rapid evolution rescues hosts from competition and disease but—despite a dilution effect—increases the density of infected hosts. Proceedings of the Royal Society B: Biological Sciences 284.

Strauss, A. T., M. S. Shocket, D. J. Civitello, J. L. Hite, R. M. Penczykowski, M. A. Duffy, C. E. Cáceres, and S. R. Hall. 2016. Habitat, predators, and hosts regulate disease in Daphnia through direct and indirect pathways. Ecological Monographs 86:393-411.