Landscape Genetics Reveals Focal Transmission of a Human Macroparasite

Macroparasite infections (e.g., helminths) remain a major human health concern. However, assessing transmission dynamics is problematic because the direct observation of macroparasite dispersal among hosts is not possible. We used a novel landscape genetics approach to examine transmission of the human roundworm Ascaris lumbricoides in a small human population in Jiri, Nepal. Unexpectedly, we found significant genetic structuring of parasites, indicating the presence of multiple transmission foci within a small sampling area (∼14 km2). We analyzed several epidemiological variables, and found that transmission is spatially autocorrelated around households and that transmission foci are stable over time despite extensive human movement. These results would not have been obtainable via a traditional epidemiological study based on worm counts alone. Our data refute the assumption that a single host population corresponds to a single parasite transmission unit, an assumption implicit in many classic models of macroparasite transmission. Newer models have shown that the metapopulation-like pattern observed in our data can adversely affect targeted control strategies aimed at community-wide impacts. Furthermore, the observed metapopulation structure and local mating patterns generate an excess of homozygotes that can accelerate the spread of recessive traits such as drug resistance. Our study illustrates how molecular analyses complement traditional epidemiological information in providing a better understanding of parasite transmission. Similar landscape genetic approaches in other macroparasite systems will be warranted if an accurate depiction of the transmission process is to be used to inform effective control strategies.Author Summary: Currently, knowledge of transmission patterns of human helminth parasites is based on traditional epidemiological data such as the number of parasites within hosts. Genetic markers can greatly facilitate our understanding of the transmission process because they provide an indirect means to infer dispersal. Here, we apply novel landscape genetics methods to examine the transmission dynamics of the world's most common human macroparasite, Ascaris lumbricoides. Specifically, we tested for both the presence of multiple transmission foci in a single human village in Nepal and the epidemiological factors associated with such infection foci. On this very local scale, we were surprised to find multiple transmission foci that were centered on households and that reinfections were occurring from the same foci. Thus, our study illustrates the utility of population genetics analyses in epidemiology. Furthermore, our study challenges current dogma by revealing fragmentation of transmission rather than homogeneous parasite mixing within a single human community. Thus, the results have important implications for drug resistance evolution and parasite control.