Personality, space use, and networks directly and indirectly explain tick infestation in a wild population of lizards

Abstract

Host personality can markedly affect parasite transmission. Especially for parasites with indirect transmission through the environment, the effects of consistent among-individual differences in behavior may have both direct and indirect components. For example, personality may mediate both how hosts respond to infected individuals and the likelihood that hosts indirectly interact with infected conspecifics (e.g., by visiting patches infected hosts have previously contaminated). Integrating parasites, personality, and these different kinds of interaction networks constitutes a key step toward understanding transmission in natural systems. We evaluated these elements using a 5-year field study of a wild population of sleepy lizards, Tiliqua rugosa, and their tick parasites, which transmit among lizards through lizards' shared use of refuges. Using Bayesian models, we evaluated (1) predictors of lizard infestation probability and intensity (i.e., average tick count when infested) and (2) relationships among the predictors. We used the latter set of models to assess indirect relationships between the predictors and the infestation metrics. As predictors, we used lizards' infestation “risk” (derived from a time-lagged refuge sharing transmission network), traits (sex, mass, and the personality axes aggression and boldness), space use (number of unique refuges used and home range overlap with other lizards), and measures of synchronous social interactions (i.e., edge weight and degree). We found both indirect and direct connections between our predictors and tick infestation. For example, boldness was positively directly associated with infection intensity and indirectly positively associated with both infestation probability and intensity via intermediary connections with social network interaction and risk. Using more unique refuges, on the other hand, was indirectly negatively associated with infestation probability (via reduced risk), but directly positively associated with infestation probability, indicating a potential trade-off in the anti-parasite benefits of using more refuges. Our results emphasize that (1) multiple aspects of host behavior may associate with parasite infection, (2) these components may proceed through both direct and indirect pathways, and (3) multiple pathways should be considered together because the pathways may have compounding or counteracting effects.