Variation in pathogen load and the pathogen load–infectiousness relationship broaden avian malaria’s distribution

The infectiousness of host species and the feeding patterns of vectors
influence pathogen distribution and transmission intensity. Two aspects of
host infectiousness shape transmission but are underappreciated: the
relationship between pathogen load and infectiousness and variability in
pathogen load within species. We quantified the relationship between host
parasitemia for avian malaria (Plasmodium relictum) and infectiousness for
biting Culex quinquefasciatus mosquitoes using experimentally infected
birds. We used this relationship and 4,218 samples from wild birds to
estimate the relative importance of hosts’ acute and chronic stages of
infection, the infectiousness of 17 bird species in Hawaiʻi, and mosquito
feeding preferences. Infectiousness to mosquitoes increased with host
parasitemia (and temperature and time since feeding), but the
relationship’s gradual slope led to a wide range of parasitemias being
partly infectious to mosquitoes. Chronic stage infections create far more
infectious mosquitoes than the acute stage, and high within-species
variability in parasitemia led to broad overlap in the infectiousness of
most bird species. Disproportionate feeding patterns (inferred from
relative infection prevalence) elevated the importance of a few bird
species in transmission, but broad overlap in species infectiousness
resulted in most host communities having similar total infectiousness.
Similar community infectiousness helped explain the widespread
distribution of avian malaria throughout Hawaiʻi despite highly variable
species communities - it was detected at 63/64 moderately well-sampled
sites. These results demonstrate the importance of the shape of the
pathogen load-infectiousness relationship and within-species variability
in pathogen load in influencing a pathogen’s host range, transmission
intensity, and spatial distribution.