Beyond single host, single parasite interactions: quantifying competence for complete multi-host, multi-parasite communities

Understanding parasite transmission in communities requires knowledge of
each species’ capacity to support transmission. This property,
“competence”, is a critical currency for modeling transmission under
community change and for testing diversity-disease theory. Despite the
central role of competence in disease ecology, we lack a clear
understanding of the factors that generate competence and drive its
variation. We developed novel conceptual and quantitative approaches to
systematically quantify competence for a multi-host, multi-parasite
community. We applied our framework to an extensive dataset: five
amphibian host species exposed to four parasitic trematode species across
five ecologically realistic exposure doses. Together, this experimental
design captured twenty host-parasite interactions while integrating
important information on variation in parasite exposure. Using
experimental infection assays, we measured multiple components of the
infection process and combined them to produce competence estimates for
each interaction. With directly estimated competence values, we asked
which components of the infection process best explained variation in
competence: barrier resistance (the initial fraction of administered
parasites blocked from infecting a host), internal clearance (the fraction
of established parasites lost over time) or pre-transmission mortality
(the probability of host death prior to transmission). We found that
variation in competence among the twenty interactions was best explained
by differences in barrier resistance and pre-transmission mortality,
underscoring the importance of host resistance and parasite pathogenicity
in shaping competence. We also produced dose-integrated estimates of
competence that incorporated natural variation in exposure to address
questions on the basis and extent of variation in competence. We found
strong signals that host species identity shaped competence variation (as
opposed to parasite species identity). While variation in infection
outcomes across hosts, parasites, individuals, and doses was considerable,
individual heterogeneity was limited compared to among-species
differences. This finding highlights the robustness of our competence
estimates and suggests that species-level values may be strong predictors
for community-level transmission in natural systems. Competence emerges
from distinct underlying processes and can have strong species-level
characteristics; thus, this property has great potential for linking
mechanisms of infection to epidemiological patterns.