Epidemiological transitions in human evolution and the richness of viruses, helminths, and protozoa

Abstract

Abstract Background and objectives In absolute terms, humans are extremely highly parasitized compared to other primates. This may reflect that humans are outliers in traits correlated with parasite richness: population density, geographic range area, and study effort. The high degree of parasitism could also reflect amplified disease risk associated with agriculture and urbanization. Alternatively, controlling for other variables, cultural and psychological adaptations could have reduced parasitism in humans over evolutionary time. Methodology We predicted the number of parasites that would infect a nonhuman primate with human phenotypic characteristics and phylogenetic position, and then compared observed parasitism of humans in eight geopolitical countries to the predicted distributions. The analyses incorporated study effort, phylogeny, and drivers of parasitism in 33 primate species. Results Analyses of individual countries were not supportive of either hypothesis. When analyzed collectively, however, human populations showed consistently lower than expected richness of protozoa and helminths, but higher richness of viruses. Thus, human evolutionary innovations and new parasite exposures may have impacted groups of parasites in different ways, with support for both hypotheses in the overall analysis. Conclusions and implications The high level of parasitism observed in humans only applies to viruses, and was not extreme in any of our tests of individual countries. In contrast, we find consistent reductions in protozoa and helminths across countries, suggesting reduced parasitism by these groups during human evolution. We propose that hygienic and technological advances might have extinguished fecal-orally or indirectly transmitted parasites like helminths, whereas higher human densities and host-shifting potential of viruses have supported increased virus richness. Lay Summary Vastly more parasite species infect humans than any other primate host. Controlling for factors that influence parasite richness, such as the intensity of study effort and body mass, we find that humans may have more viruses, but fewer helminths and protozoa, than expected based on evolutionary analyses of parasitism in other primates.