Parasitic infection manipulates intermediate host behaviour in a social carnivore

We studied the effects of Toxoplasma gondii on wolf behaviour in Yellowstone National Park, Wyoming, USA. We found that seropositive wolves were more likely to make high-risk decisions such as dispersing and becoming a pack leader, both factors critical to individual fitness and wolf vital rates.
Published in Ecology & Evolution
Parasitic infection manipulates intermediate host behaviour in a social carnivore
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I was sitting in a packed lecture hall, one of sixty students in Dr. Aaron Wirsing's freshman level "Wildlife in the Modern World" course, when Dr. Wirsing booming voice reverberated throughout the auditorium: "For all the focus there is on how big carnivores impact prey behavior, we may be looking in the wrong place, perhaps it's the small things driving wildlife behavior and decision making". We know that no single factor drives animal decision-making, but Dr. Wirsing was referencing the then-recent research on the protozoan parasite Toxoplasma gondii. At the time T. gondii made headlines in popular media for being the "crazy cat lady parasite," where humans exposed to the parasite exhibited increased attraction to felid urine, compared to uninfected humans. Without knowing it, this lecture set the stage for our recent publication, almost 10 years later.

Toxoplasma gondii is a protozoan parasite capable of infecting any warm-blooded species on the planet. It's multi-host life cycle relies on its definitive host (a felid) ingesting infected muscle tissue of prey animals. In felids, once ingested T. gondii sexually reproduces in the gut before infectious oocysts are deposited in the environment along with feces. These oocysts can survive for up to and over a year, depending on the environment. In non-felid mammals, once either infected oocysts or infected muscle tissue of prey animals are ingested, infection crosses the gut and moves to the newly infected hosts muscle tissue, waiting to be ingested, and to the brain, where it interacts with hormone production. In observational human and experimental rodent studies, T. gondii exposure correlates to increased testosterone (Lim et al. 2013, Zouei et al. 2018) and dopamine production (Stibbs 1985, McConkey et al. 2013). This hormone alteration can manifest as behavioral changes including increased aggression (Arnott et al. 1990, Coccaro et al. 2016) and increased risky decision-making including increased hyperactive movement, failure to avoid olfactory predator cues (i.e., seeking out instead of avoiding felid urine), and decreased neophobia (Lim et al. 2013, Webster et al. 1994, Berdoy et al. 2000, Poirotte et al. 2016). It is theorized that the increased risky decision making induced by T. gondii cysts on the brains of infected intermediate hosts increases predation by felids, and hence parasite transmission.

Years later, while working for the Yellowstone Wolf and Cougar Projects to understand interspecific competition and predator-prey dynamics between wolves, cougars, and elk, Dr. Wirsing's booming voice continued on repeat in my head "perhaps it’s the little things controlling the system". I soon began discussing parasitic manipulation with co-lead author Kira Cassidy, and co-author Erin Stahler. We worked for one of the best wildlife studies in the world to understand the role that T. gondii may play in ecosystem interactions. At the same time, a recent publication out of the Mara Hyena Project, where exposure to T. gondii led to increased behavioral boldness and increased probability of lion-caused mortality in spotted hyenas (Gering et al. 2021). That study was the first of its kind in wild large carnivore hosts, and suggested a definitive link between T. gondii infection, behavioral boldness, and risk taking.

Following previous research on disease dynamics in the Yellowstone National Park wolf population we knew that wolves had been exposed to T. gondii (Brandell et al. 2021). What we didn't know however, was what factors drove T. gondii infection, and if exposure to T. gondii affected wolf behavior. The stage was set, and we dove straight in. 

Panel a: Map of cougar density and T. gondii seroprevalence in wolves in Yellowstone National Park (YNP). Yellow indicates cougar density <1.8/100 km2 and purple indicates cougar density ≥1.8/100km2. Pie charts show the T. gondii seroprevalence (seropositive=black; seronegative=white/transparent) from wolves living in nine general areas throughout YNP, pooled across years 2000-2020. Panel b: A sample year (2015) of wolf pack territory minimum convex polygons in YNP along with each pack’s cougar overlap index level (LCO, MCO, or HCO) based on percentage of overlap with cougar density ≥1.8/100km2 (purple)

Panel a: Map of cougar density and T. gondii seroprevalence in wolves in Yellowstone National Park (YNP). Yellow indicates cougar density <1.8/100 km2 and purple indicates cougar density ≥1.8/100km2. Pie charts show the T. gondii seroprevalence (seropositive=black; seronegative=white/transparent) from wolves living in nine general areas throughout YNP, pooled across years 2000-2020. Panel b: A sample year (2015) of wolf pack territory minimum convex polygons in YNP along with each pack’s cougar overlap index level (LCO, MCO, or HCO) based on percentage of overlap with cougar density ≥1.8/100km2 (purple)

First, we tested whether individual age, sex, social status, coat color, and/or a metric of wolf pack overlap with cougars predicted exposure to T. gondii. Contrary to previous studies, our results did not indicate that likelihood of exposure to T. gondii increased over time, nor that individual sex (based on external reproductive organs) had a large effect on its own. The most important predictor was our metric of annual wolf pack territory with areas in YNP where cougar density was greater than or equal to 1.8 cougars/100 km2. We estimate that a wolf with low cougar overlap has a ~4% probability of testing positive for toxoplasmosis (the disease caused by T. gondii), medium overlap ~12% and a wolf with high annual pack territory overlap with cougar density is 28%.  So, wolves living in areas with T. gondii’s definitive host are more likely to get infected than wolves in areas with fewer felids.

Gray wolves with T. gondii serology results were divided into one of three categories relative to their average annual overlap with cougar density ≥1.8/100km2 (top bar): Low Cougar Overlap (LCO in yellow) indicates wolves living in areas with 0.0 to 5.0% overlap, Moderate Cougar Overlap (MCO in orange) indicates 5.1-42.0% overlap, and High Cougar Overlap (HCO in red) indicates 42.1-100% overlap. This results in three categories of nearly equal sample size. The lower bars show the predicted probabilities, with 95% confidence intervals, of a seropositive T. gondii test for gray wolves living in LCO (yellow), MCO (orange), or HCO (red). Predicted probabilities are based on the full model

Gray wolves with T. gondii serology results were divided into one of three categories relative to their average annual overlap with cougar density ≥1.8/100km2 (top bar): Low Cougar Overlap (LCO in yellow) indicates wolves living in areas with 0.0 to 5.0% overlap, Moderate Cougar Overlap (MCO in orange) indicates 5.1-42.0% overlap, and High Cougar Overlap (HCO in red) indicates 42.1-100% overlap. This results in three categories of nearly equal sample size. The lower bars show the predicted probabilities, with 95% confidence intervals, of a seropositive T. gondii test for gray wolves living in LCO (yellow), MCO (orange), or HCO (red). Predicted probabilities are based on the full model.

Next, we identified three behaviors: 1) Dispersal from one's natal pack; 2) Becoming a pack leader; 3) Approaching people or vehicles (deemed "habituation") and two causes of death: a) being killed by other wolves (i.e., intraspecific mortality); b) being killed by people (i.e., anthropogenic mortality) that could be deemed "risky" for wolves. From here we built generalized linear mixed models to predict how demographic covariates including sex (based on external reproductive organs), system (where in YNP wolves lived, either in the park interior or on the northern range of YNP), amount of time monitored (as a proxy for age) and T. gondii serostatus. 

To our surprise, T. gondii serostatus was an important predictor of leadership and dispersal behavior in wolves but was not important for predicting habituated behavior or a cause of death. T. gondii may be less important for these behaviors as habituation, human-caused and wolf-caused mortality are indicative of behaviors that wolves, being a social species, may learn from conspecifics and therefore not as predictable in regards to T. gondii infection. 

Our results regarding T. gondii serostatus effect on predicting dispersal and leadership behaviors was significant--wolves that were seropositive for T. gondii were 11 times more likely to disperse and 46 times more likely to become a leader

Schematic of results from both the demographic and the behaviour analysis. Displayed at the top are three sample packs with different cougar overlap categories and their corresponding predicted probabilities of T. gondii infection (seronegative in black; seropositive in red) based on the best-fit demographic model. Red-filled wolves indicate the expected percent of infected wolves out of 100%. Cougar density ≥1.8/100km2 is depicted with hatch-marks. Cougar density below 1.8/100km2 is all the area outside of the hatch-marks. At the bottom are the predicted probabilities with 95% confidence intervals (gray lines) based on the best-fit behaviour models, of two risky behaviours: dispersing and becoming a pack leader for seronegative and seropositive wolves at 24.9 months monitored (the average number of months wolves in this study were monitored)

These results indicate that T. gondii serostatus can have an enormous impact on wolf behavior and population dynamics. Given wolves’ ability to affect ecosystem processes and social learning, T. gondii's effect on wolf behavior may ripple beyond the infected individuals. Seropositive individuals being more likely to disperse and/or become pack leaders may increase breeding opportunities for infected individuals. Even though vertical transmission of T. gondii (mother to offspring) is very unlikely, wolves that are leaders are usually the ones in the pack that are producing offspring, a great benefit for achieving that social position. Since T. gondii infection influences the likelihood of becoming a leader, the parasite is indirectly impacting important vital rates. We are just beginning to learn more about social learning in group living species, where knowledge is passed to conspecifics, generally from older individuals, or those in leadership positions. If wolf pack leaders are more likely to have contracted toxoplasmosis, they may lead uninfected packmates into situations where transmission risk increases or, may teach risky behaviors to uninfected packmates, without a change in T. gondii serostatus.  

Schematic of the possible feedback loop involving gray wolves, cougars, and T. gondii. Red figures indicate seropositive animals and black indicates seronegative animals. Thick, purple arrows indicate links supported by this or other published literature. Thin, gray lines indicate hypothesized relationships.

Just as Dr. Aaron Wirising told me back in 2012, "perhaps it is the small things running the world." Given our results, and the possible implications of T. gondii infection in the wild, now published for spotted hyenas and gray wolves, we implore anyone studying animal behavior and ecology to consider the effects of parasitic infection. Untangling the complex web of ecosystem interactions and interspecies relationships might just come down to the little things. 

Acknowledgements:

This article was written by C.Meyer with input and edits provided by K. Cassidy. I additionally acknowledge that Yellowstone National Park is situated in the aboriginal homelands and/or is of cultural significance to many indigenous tribes, including the Assiniboine and Sioux, Blackfeet, Cheyenne River Sioux, Coeur d’Alene, Comanche, Colville Reservation, Crow, Crow Creek Sioux, Eastern Shoshone, Flandreau Santee Sioux, Gros Ventre and Assiniboine, Kiowa, Little Shell Chippewa, Lower Brule Sioux, Nez Perce, Northern Arapaho, Northern Cheyenne, Oglala Sioux, Rosebud Sioux, Salish and Kootenai, Shoshone–Bannock, Sisseton Wahpeton, Spirit Lake, Standing Rock Sioux, Turtle Mountain Band of the Chippewa, Umatilla Reservation, and Yankton Sioux people.

Citations: 

Arnott, M.A., Cassella, J.P., Aitken, P.P. & Hay, J. (1990). Social interactions of mice congenital Toxoplasma infection. Ann Trop Med Parasitol, 84, 149–156.

Berdoy, M., Webster, J.P. & Mcdonald, D.W. (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society B: Biological Sciences, 267, 1591–1594.

Brandell, E.E., Cross, P.C., Craft, M.E., Smith, D.W., Dubovi, E.J., Gilbertson, M.L.J., et al. (2021). Patterns and processes of pathogen exposure in gray wolves across North America. Sci Rep, 11.

Coccaro, E.F., Lee, R., Groer, M.W., Can, A., Coussons-Read, M. & Postolache, T.T. (2016). Toxoplasma gondii infection: Relationship with aggression in psychiatric subjects. Journal of Clinical Psychiatry, 77, 334–341.

Gering, E., Laubach, Z.M., Weber, P.S.D., Soboll Hussey, G., Lehmann, K.D.S., Montgomery, T.M., et al. (2021). Toxoplasma gondii infections are associated with costly boldness toward felids in a wild host. Nat Commun, 12.

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McConkey, G.A., Martin, H.L., Bristow, G.C. & Webster, J.P. (2013). Toxoplasma gondii infection and behaviour - Location, location, location? Journal of Experimental Biology, 216, 113–119.

Poirotte, C., Kappeler, P.M., Ngoubangoye, B., Bourgeois, S., Moussodji, M. & Charpentier, M.J.E. (2016). Morbid attraction to leopard urine in toxoplasma-infected chimpanzees. Current Biology.

Stibbs, H.H. (1985). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol, 79, 153–157.

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Zouei, N., Shojaee, S., Mohebali, M. & Keshavarz, H. (2018). The association of latent toxoplasmosis and level of serum testosterone in humans. BMC Res Notes, 11.

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