Landscape Genetics Reveals Focal Transmission of a Human Macroparasite

Abstract

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.

Prediction and Prevention of Parasitic Diseases Using a Landscape Genomics Framework

“…The spread of parasitic disease, however, has drawn only limited attention from the field. Pioneered by work on rabies [11] and chronic wasting disease [12], research has targeted a handful of viruses (reviewed in [13]; see also [14]) and microbes (notably Batrachochytrium dendrobatidis [15]), helminths with direct life cycles [16,17] and their hosts. Systems involving vector-borne pathogens [18–21] or several intermediate hosts [22] have been mostly spared from investigation.…”

Genetic Epidemiology of Ascaris

“…6 In the case of Ascaris, adult worms would be genotyped from human hosts. 41 The goals of the study by Criscione and colleagues 41 were to determine if there was more than one source pool of infection (i.e. I refer readers to Steinauer and colleagues 37 for a more thorough discussion of this type of sampling.…”

Ascaris lumbricoides

“…Molecular analysis of worms from the same Nepalese community showed genotypic clustering of worms infecting members of the same household, suggesting that households, at least in this community, are important transmission foci (Chapter 8). 82 The importance of the household in the transmission of A. lumbricoides and T. trichiura e and to a lesser extent hookworm e was first identified in the late 1920s to early 1930s from work conducted in China, 83 Panama 84 and the southern United States of America. 85 These ideas were revisited by Williams et al in 1974 86 and by others in the late 1980s 81 and early 1990s, 87 and expounded in 1996 by Cairncross et al 88 who described the household (for Ascaris and Trichuris) and the public environments (for hookworm) as "fundamental arenas of disease transmission.…”