Population genomics reveals multi-scale mechanisms sustaining schistosomiasis re-emergence in a near-elimination setting
6 affiliations
- 1Department of Biology, University of Texas at Arlington, Arlington, Texas, United States of America
- 2Department of Environmental and Occupational Health, Colorado School of Public Health, University of Colorado Anschutz, Aurora, Colorado, United States of America
- 3Department of Neurology, Weill Institute for Neurosciences, University of California San Francisco, San Francisco, California, United States of America
- 4Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel
- 5Sichuan Center for Disease Control and Prevention, Chengdu, The People’s Republic of China
- 6Department of Biochemistry & Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America
Abstract
In China, sustained snail control, environmental management, and mass drug administration with praziquantel reduced schistosomiasis to near-elimination levels, yet re-emergence in Sichuan Province during the early 2000s exposed vulnerabilities in elimination efforts. We used population genomics to investigate the multi-scale population processes underlying Schistosoma japonicum re-emergence in Sichuan. We sequenced whole genomes from 270 miracidia collected from 53 human hosts across 17 villages in 2007, one year after re-emergence was documented. Population genomic analyses identified a broadly cohesive regional schistosome population with weak geographic structuring. Genome-wide diversity remained substantial, and demographic reconstructions revealed no recent decline in effective population size, suggesting that parasite populations had not undergone regional demographic collapse prior to re-emergence and were likely maintained in non-human reservoir hosts. At finer spatial scales, several villages exhibited reduced genomic diversity and elevated inbreeding, consistent with localized transmission maintained by relatively small founding populations. Estimates of pairwise genetic relatedness revealed dense within-village sibling clusters alongside second- and third-degree relationships spanning villages, and rare first- and second-degree cross-village links, supporting predominantly local transmission embedded within a connected regional transmission network. Genomic inference of minimum reproducing worm pairs identified substantial heterogeneity in host-level worm burden, ranging from one to eleven adult worm pairs, although uneven sampling limited absolute estimates. Together, these findings indicate that parasite persistence in this near-elimination setting was sustained by interacting processes operating across multiple biological scales, including diverse regional parasite populations, localized transmission networks connecting villages, and marked heterogeneity in host-level worm burden. More broadly, this work demonstrates how population genomics can reconstruct otherwise hidden patterns of parasite persistence and transmission, providing a valuable complement to conventional epidemiological surveillance in complex, multi-host parasite systems. Author summary: Schistosomiasis is a parasitic disease that affects millions of people worldwide. Understanding the factors that sustain parasite persistence and transmission, even in the face of control programs, is central to reducing and ultimately eliminating the disease. In China, decades of intensive control efforts have dramatically reduced infections, yet schistosomiasis persisted and re-emerged in some regions. In this study, we analyzed the genomes of 270 S. japonicum larvae collected from infected humans across 17 villages in Sichuan Province, China, shortly after schistosomiasis re-emerged in the region. Using population genomic analyses, we reconstructed the population processes underlying parasite persistence and transmission across regional, village, and host scales. Our findings suggest that, despite major reductions in human infection prevalence, schistosome population sizes do not show signatures of recent population decline, indicating that non-human hosts likely contributed to schistosomiasis persistence. Genetic relatedness among parasites also revealed that transmission remained highly localized, with relatively few infected snail hosts contributing disproportionately to infections within villages. Collectively, these findings suggest that parasite persistence reflected interacting processes operating across multiple biological scales, including non-human reservoirs, regional connectivity, localized transmission networks, and heterogeneous host-level worm burdens, highlighting challenges for elimination and demonstrating the value of population genomics for genomic surveillance.
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BibTeX
@article{guss2026population,
title = {{Population genomics reveals multi-scale mechanisms sustaining schistosomiasis re-emergence in a near-elimination setting}},
author = {Hannah D. Guss and Yannick Z. Francioli and Elise N. Grover and Andrew Hill and Wei Zou and Kristen J. Wade and Hamish Pike and Siddharth S. Gopalan and Liu Yang and Zhong Bo and David D. Pollock and Elizabeth J. Carlton and Todd A. Castoe},
journal = {PLOS Neglected Tropical Diseases},
year = {2026},
month = sep,
doi = {10.1371/journal.pntd.0014202},
url = {https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0014202},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Population genomics reveals multi-scale mechanisms sustaining schistosomiasis re-emergence in a near-elimination setting
AU - Hannah D. Guss
AU - Yannick Z. Francioli
AU - Elise N. Grover
AU - Andrew Hill
AU - Wei Zou
AU - Kristen J. Wade
AU - Hamish Pike
AU - Siddharth S. Gopalan
AU - Liu Yang
AU - Zhong Bo
AU - David D. Pollock
AU - Elizabeth J. Carlton
AU - Todd A. Castoe
PY - 2026
DA - 2026/09/08
JO - PLOS Neglected Tropical Diseases
DO - 10.1371/journal.pntd.0014202
UR - https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0014202
AB - In China, sustained snail control, environmental management, and mass drug administration with praziquantel reduced schistosomiasis to near-elimination levels, yet re-emergence in Sichuan Province during the early 2000s exposed vulnerabilities in elimination efforts. We used population genomics to investigate the multi-scale population processes underlying Schistosoma japonicum re-emergence in Sichuan. We sequenced whole genomes from 270 miracidia collected from 53 human hosts across 17 villages in 2007, one year after re-emergence was documented. Population genomic analyses identified a broadly cohesive regional schistosome population with weak geographic structuring. Genome-wide diversity remained substantial, and demographic reconstructions revealed no recent decline in effective population size, suggesting that parasite populations had not undergone regional demographic collapse prior to re-emergence and were likely maintained in non-human reservoir hosts. At finer spatial scales, several villages exhibited reduced genomic diversity and elevated inbreeding, consistent with localized transmission maintained by relatively small founding populations. Estimates of pairwise genetic relatedness revealed dense within-village sibling clusters alongside second- and third-degree relationships spanning villages, and rare first- and second-degree cross-village links, supporting predominantly local transmission embedded within a connected regional transmission network. Genomic inference of minimum reproducing worm pairs identified substantial heterogeneity in host-level worm burden, ranging from one to eleven adult worm pairs, although uneven sampling limited absolute estimates. Together, these findings indicate that parasite persistence in this near-elimination setting was sustained by interacting processes operating across multiple biological scales, including diverse regional parasite populations, localized transmission networks connecting villages, and marked heterogeneity in host-level worm burden. More broadly, this work demonstrates how population genomics can reconstruct otherwise hidden patterns of parasite persistence and transmission, providing a valuable complement to conventional epidemiological surveillance in complex, multi-host parasite systems. Author summary: Schistosomiasis is a parasitic disease that affects millions of people worldwide. Understanding the factors that sustain parasite persistence and transmission, even in the face of control programs, is central to reducing and ultimately eliminating the disease. In China, decades of intensive control efforts have dramatically reduced infections, yet schistosomiasis persisted and re-emerged in some regions. In this study, we analyzed the genomes of 270 S. japonicum larvae collected from infected humans across 17 villages in Sichuan Province, China, shortly after schistosomiasis re-emerged in the region. Using population genomic analyses, we reconstructed the population processes underlying parasite persistence and transmission across regional, village, and host scales. Our findings suggest that, despite major reductions in human infection prevalence, schistosome population sizes do not show signatures of recent population decline, indicating that non-human hosts likely contributed to schistosomiasis persistence. Genetic relatedness among parasites also revealed that transmission remained highly localized, with relatively few infected snail hosts contributing disproportionately to infections within villages. Collectively, these findings suggest that parasite persistence reflected interacting processes operating across multiple biological scales, including non-human reservoirs, regional connectivity, localized transmission networks, and heterogeneous host-level worm burdens, highlighting challenges for elimination and demonstrating the value of population genomics for genomic surveillance.
SN - 1935-2735
ER -