Question

What information would you need to compare tolerance among sheep? How would you determine if one sheep was more tolerant than another? Draw a graph that illustrates the tolerance of several individual sheep.

Answer 1

NATIONAL CENTER FOR CASE STUDY TEACHING IN SCIENCE Coping with Infection: Resistance and Tolerance of Parasites in Soay Sheep Laura A. Schoenle, Cornell University, Ithaca, NY Cynthia J. Downs, Hamilton College, Clinton, NY Part 1 - Sheep and Their Parasites About 70 kilometers west of mainland Scotland lies the archipelago of St. Kilda, home to the Soay sheep (Ovis aries) (Figure 1). Soay sheep are the most primitive domesticated sheep in Europe, and they resemble the domesticated sheep farmed during the Neolithic era (circa 5000 BCE) (Boyd et al., 1964). A Figure 1 (A). Adult Soay sheep. Credit: Velmc, CC BY-NC 2.0. Figure 1 (B). Soay lamb. Credit: marcus_jb1973, CC BY-NC-ND 2.0. An unmanaged population of Soay sheep continues to live on the island of Hirta, St. Kilda. The popula- tion size varies dramatically across years, ranging from about 600 to 1600 individuals (Clutton-Brock et al., 1991; Coulson et al., 2001). Over the winter, there can be high mortality of adult sheep, primarily due to star- vation. Starvation is not only caused by lack of food, but is intensified by infections with multiple species of gastrointestinal nematodes (Figure 2) (Gulland, 1992). Nematode infections increase mortality rates in Soay sheep, and the intensity of infection (the number of infecting worms, which is estimated by the number of nematode eggs in sheep feces) correlates negatively Figure 2. A common parasitic gastrointestinal nematode of sheep, Teladorsagia circumcinta. Credit: Bartley et al. (2015), CC BY-NC-ND 4.0. cs Case copyright held by the National Center for Case Study Teaching in Science, University at Buffalo, State University of New York. Originally published November 29, 2018. Please see our usage guidelines, which outline our policy concerning permissible reproduction of this work. Photo in title block of Spay sheep grazing on St. Kilda by Allan MacDonald/amdphoto.co.uk, used with permission. Acknowledgements: LAS and CJD were supported by NSF grants IOS-1656551 (to CJD). LAS was also supported by IOS-1656618 (to LB Martin). CamScanner

NATIONAL CENTER FOR CASE STUDY TEACHING IN SCIENCE 22.5 . with sheep body mass (Figure 3). Because nematodes reduce survival, natural selection is expected to shape how the sheep cope with nematode infections. There are two strategies for coping with parasite infec- tions: resistance and tolerance (Schneider & Ayres, 2008; Råberg, Graham & Read, 2009). Resistance involves controlling the number of parasites by avoid- ing the infection, killing or removing parasites, or limiting the parasites' ability to reproduce in the host. Tolerance involves minimizing the costs of infection or controlling the damage caused during infection. For more background on resistance and tolerance see Sch- neider and Ayres (2008), and Medzhitov, Schneider and Soares (2012). Mean body weight (kg) 10.04 0 2000 400 800 1200 1600 Strongyle FEC (eggs/gram) Questions Figure 3. Sheep with higher fecal egg counts (FEC) of strongyle nema- todes weigh less than sheep with lower egg counts. The negative rela- tionship between body weight and FEC shown here is based on data of 4,934 captures of 2,438 individual sheep. Points show the mean body weight + 1 standard error. Figure reproduced from Hayward et al. (2014b), CC BY-NC-ND 4.0. 1. Imagine you are studying Soay sheep on the island of Hirta. How would you compare resistance among sheep? In other words, what would you need to know to rank sheep by their resistance to nematodes? 2. What information would you need to compare tolerance among sheep? How would you determine if one sheep was more tolerant than another? Draw a graph that illustrates the tolerance of several individual sheep. (Hint: Figure 3 and the background readings might provide inspiration.) 3. Do you expect sheep that invest more in resistance to nematodes or tolerance of nematodes to be more likely to survive over the winter? Why? 4. Imagine you are a nematode that infects Soay sheep. If you want to maximize the likelihood that you survive and reproduce, should you prefer a more resistant sheep host or more tolerant host? Why? Page 2 "Coping with Infection" by Schoenle and Downs Scanned with CamScanner

NATIONAL CENTER FOR CASE STUDY TEACHING IN SCIENCE Body weight (kg) T 0 500 1000 2000 Strongyle FEC (eggs/gram) Part II - The Costs and Benefits of Immunity to Parasites Soay sheep can resist gastrointestinal nematode infections by mounting an immune response. Sheep that produce more antibodies to a common nematode (shown in Figure 2) have fewer intestinal nematodes than sheep producing less antibodies (Hayward et al., 2014a). These antibodies have complex relationships with two measures of fitness: survival probability and reproductive success. Among female sheep, producing more antibodies causes an increase in survival during years when there is high overwinter mortality (a population crash), but not during years with relatively low overwinter mortality (no population crash) (Graham et al., 2010). In males, there is no relationship between antibodies and survival (Graham et al., 2010). However, males with higher antibody levels are less likely to father offspring the following year than males with lower antibody levels (Graham et al., 2010; Hayward et al., 2014a). Similarly, females with higher antibody levels produce fewer lambs than females with lower antibody levels (Graham et al., 2010), but the effects can vary depending on female body mass (Hay- ward et al., 2014a). A study by Hayward et al. (2014b) focused on Soay sheep tolerance of nema- todes, and measured tolerance as the slope of the relationship between body weight and fecal egg count (Figure 4). They found that sheep with higher tolerance had higher lifetime breeding success (Figure 5). This means that sheep that were better able to maintain their body weight when carrying more parasites had higher reproductive success. Figure 4. Tolerance can be measured as the slope of the relationship between body weight and fecal egg count. Each line represents an individual sheep sampled at multiple points during its lifetime. Figure reproduced from Hayward et al. (2014b), CC BY-NC-ND 4.0. Mean relative LBS Questions 1. Do higher levels of antibodies indicate greater resistance to nematodes in Soay sheep? Explain your answer. Can the relationship between antibodies and resistance in the sheep be generalized to other host-parasite systems? 1 4 2 3 Tolerance quartile 2. The work described here is correlational, and thus cannot determine if the relationship between two variables is causal. Design an experiment that tests whether antibodies cause greater resistance to nematodes in Soay sheep, and list specific predictions. Figure 5. The relationship between toler- ance and lifetime breeding success (LBS). Figure reproduced from Hayward et al. (2014b), CC BY-NC-ND 4.0. 3. What appear to be the costs of higher antibody levels? Why might higher antibody levels have negative consequences? 4. Yikes, it's complicated! The relationship between antibody levels and fitness seems to vary by context. Why might this be the case? 5. Tolerance is also associated with reproductive success. Under what conditions might an animal benefit from investing more in tolerance? Under what conditions might an animal benefit by investing more in resistance? 6. Consider how doctors and veterinarians treat parasites (including viruses, bacteria, worms, lice, etc.). Is modern medicine more focused on resistance or tolerance? Why? Page 3 "Coping with Infection" by Schoenle and Downs Scanned with CamScanner