Host preferences inhibit transmission from potential superspreader host species.

Host species that are particularly abundant, infectious and/or infected tend to contribute disproportionately to symbiont (parasite or mutualist) maintenance in multi-host systems. Therefore, in a facultative multi-host system where two host species had high densities, high symbiont infestation intensities and high infestation prevalence, we expected interspecific transmission rates to be high. Instead, we found that interspecific symbiont transmission rates to caged sentinel hosts were an order of magnitude lower than intraspecific transmission rates in the wild. Using laboratory experiments to decompose transmission rates, we found that opportunities for interspecific transmission were frequent, where interspecific and intraspecific contact rate functions were statistically indistinguishable. However, most interspecific contacts did not lead to transmission events owing to a previously unrecognized transmission barrier: strong host preferences. During laboratory choice experiments, the symbiont preferred staying on or dispersing to its current host species, even though the oligochaete symbiont is a globally distributed host generalist that can survive and reproduce on many snail host species. These surprising results suggest that when managing symbiont transmission, identifying key host species is still important, but it may be equally important to identify and manage transmission barriers that keep potential superspreader host species in check.

Handling times and saturating transmission functions in a snail-worm symbiosis.

All dynamic species interaction models contain an assumption that describes how contact rates scale with population density. Choosing an appropriate contact-density function is important, because different functions have different implications for population dynamics and stability. However, this choice can be challenging, because there are many possible functions, and most are phenomenological and thus difficult to relate to underlying ecological processes. Using one such phenomenological function, we described a nonlinear relationship between field transmission rates and host density in a common snail-oligochaete symbiosis. We then used a well-known contact function from predator-prey models, the Holling Type II functional response, to describe and predict host snail contact rates in the laboratory. The Holling Type II functional response accurately described both the nonlinear contact-density relationship and the average contact duration that we observed. Therefore, we suggest that contact rates saturate with host density in this system because each snail contact requires a non-instantaneous handling time, and additional possible contacts do not occur during that handling time. Handling times and nonlinear contact rates might also explain the nonlinear relationship between symbiont transmission and snail density that we observed in the field, which could be confirmed by future work that controls for other potential sources of seasonal variation in transmission rates. Because most animal contacts are not instantaneous, the Holling Type II functional response might be broadly relevant to diverse host-symbiont systems.