Our tiny predators: Using ecology to understand and teach infectious disease Shelby Williams Loberg a,*, Clarence Lehman a Contact information: a: Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108; * Corresponding author: [email protected]

1 species

Examine the ecology of infectious disease from a one-, two-, and three-species perspective, as well as from an ecosystem perspective:

As the human population increased, we transitioned from frequency-dependent diseases to include density-dependent diseases. Density- and frequencydependent diseases have different qualities. Given these qualities, we developed a class activity where the students tried to determine which diseases our hunter-gatherer ancestors likely suffered.

Interactions between two species can be simpli1ied into one of the categories shown on the left. The categories are based on whether Species 1 harms, helps, or is indifferent to Species 2, and vice versa.

Ecosystem

3 species

2 species

Rather than battle predators directly, we can develop relationships with mutualists to reduce pathogens.

Infectious diseases overlap with concepts of ecosystem ecology as well. Below are three case studies we used in our class. Habitat destruction and vaccination are the same



(Tilman, May, Lehman,and Nowak, 1994)

Bacteria as predators. Until 1928 humans suffered as prey for bacteria, while Penicillium molds were able to compete successfully with certain bacteria. bacteria

Red points to a predator, blue points to a superior competitor penicillium

“The enemy of my enemy is my friend.” Humans purposefully increased and focused the population of Penicillium mold to help us combat bacteria. We do this when we set up a mutualism with Penicillium mold, which is a competitor with human pathogens.

Human population estimates since 12,000 BP. Changes in worldwide temperatures 10,000 years ago accompanied agriculture and corresponding lifestyles. Groups became sedentary and densely populated, leading to a different category of disease, the so-called density-dependent diseases. Match the traits below to the table cells. Pre-agriculture traits High transmission Low virulence Little to no immunity Reservoirs common Chronic diseases common Vector-borne common

Post-agriculture traits Low transmission High virulence/recovery Associated with domestic animals Acute diseases common (Dobson and Carper, 1996)

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The isomorphism between habitat destruction (top equation) and vaccination (bottom equation) means that conclusions from one model, including equilibrium, effects of vaccination, and evolution of virulence and infectivity, have exact parallels in the other model.

Unintended consequences of hygiene After the horse-drawn era, manure vanished, running water arrived along with Clush toilets, hygiene improved, sealed screen doors became common, and Clies died in vast numbers. Thus the fecal–oral pathway diminished and the infectivity of related diseases fell. As the chance of catching polio decreased, the average age of onset increased. Vaccines became available in the late 1950s.

bacteria

One of the more difCicult concepts for students to grasp, in our experience, is that positive and negative relationships or growth is on the population level, rather than the individual level. For example, even though humans eventually harvest individual livestock such as cattle, their population has increased because of humans, signifying a mutualism between livestock and humans.

Green joins mutualists

penicillium

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Example of applying this theory

We battle our tiny predators by switching our ecological interactions with them from predator-prey (Fig. B) to competition (Fig. A) or mutualism (Fig. C).

Predation to Competition. An example of competition is the successful eradication of smallpox in the natural world. According to Dr. William Foege, who helped orchestrate the eradication, we humans evolved faster than the smallpox pathogen.

Predation to Mutualism. On the other hand, we may be able to “domesticate germs” as proposed by Dr. Paul Ewald. He explains how cholera in South America was domesticated on an evolutionary basis by forcing the pathogens from a water-borne illness to a person-to-person transmission.

Other mutualists we’ve cultivated. The “penicillium” node could also be phages for a virus predator. viruses Red points to a predator, blue points to a superior competitor, green joins mutualists phages

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Nathanson and Kew, 2010

Diversity and dilution Students learned the effects of antibiotics on gut microbial diversity, and the subsequent potential of C. dif1icile infection. Students measured diversity using Shannon Diversity Index and made predictions about antibiotic Antibiotic treated gut vs. control effects. Loberg et al. submitted Jakobsson et al. 2010

Table from Wolfe et al. 2007, Supplemental table S1

This project was supported in part by financial awards from the University of Minnesota’s Provost Office Grand Challenge Course, the College of Biological Sciences, and the Institute on the Environment.

Hosts as ponds We found that a useful thought experiment for students was abstracting hosts– including human, plants, or other animals– into ecological “ponds,” and parasites into ecological “pond-dwellers.” It reduced the complexity of pathogen physiology and behavior and helped us focus on the essentials of pathogens by comparing them to the ecology of “pond-dwellers,” including: a.  Surviving and reproducing in the pond b.  Getting to another pond (or their offspring) c.  Not fouling the pond before some get to another pond

Background of the course

Caveats to the predation analogy Equating our pathogens to “tiny predators” has many beneCits as illustrated on this poster, but there are important differences between predators and pathogens. Some of these are: 1.  2.  3.  4.  5. 

Disease organism is not independently mobile. Disease organism doesn’t necessarily kill its victim. After infection with a disease organism, victim may become immune. Disease organism is very much smaller than its victim. Discussion of certain aspects of certain diseases can be more indelicate than discussions of predator–prey interactions. Image: petattack.com

In 2015, the authors co-designed and co-instructed a new course at the University of Minnesota. The course was titled Our Tiny Predators: Ecology, Infection, and Disease, and was well-attended and received by an interdisciplinary group of undergraduate students. We incorporated activities shown in this chart as well as active learning principles.

In 2016, an expanded version of this course will be offered as a Grand Challenge Course at the University of Minnesota. We are seeking feedback on this poster to improve that course. www.postersession.com