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

Abstract

Two aspects of host infectiousness shape pathogen transmission and distribution but are underappreciated: the relationship between pathogen load and infectiousness, and variability in pathogen load within species. We quantified the relationship between host pathogen load (parasitemia) for avian malaria (Plasmodium relictum) and infectiousness for biting Culex quinquefasciatus mosquitoes with experimental infections in canaries (Serinus canaria). Using this relationship, we estimated the infectiousness of 17 bird species in 11 communities in Hawaiʻi and quantified the relative contributions of infection stage (acute versus chronic) to transmission. We show that infectiousness to mosquitoes increased with parasitemia, temperature, and time since feeding. The relationship’s gradual (low) parasitemia slope resulted in a wide range of parasitemias being partly infectious, and high within-host species variability in parasitemia led to extensive overlap in infectiousness among hosts. Disproportionate mosquito host utilization (inferred from relative infection prevalence) elevated the importance of a few host species, yet broad overlap in species infectiousness resulted in similar total infectiousness across most bird communities. This similarity likely contributed to avian malaria’s widespread distribution throughout Hawaiʻi despite diverse host community assemblages. Our findings highlight the importance of both the shape of the pathogen load–infectiousness relationship and within-species variability in determining a pathogen’s host range, transmission intensity, and spatial spread.