Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years

China was once a major endemic zone for Schistosoma japonicum, but decades of control efforts have dramatically reduced transmission. Suzhou City, in Jiangsu Province, a former hyperendemic area, achieved transmission interruption in 1995. However, the intermediate host Oncomelania hupensis persists...

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Main Authors: Liu Ze-Ting, Peng Han-Qi, Qi Yu-Xin, Wu Xiao-Yan, Xu Qing, Zhang Han-Xiang, Lu Da-Bing
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Language:English
Published: EDP Sciences 2025-01-01
Series:Parasite
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Online Access:https://www.parasite-journal.org/articles/parasite/full_html/2025/01/parasite250009/parasite250009.html
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author Liu Ze-Ting
Peng Han-Qi
Qi Yu-Xin
Wu Xiao-Yan
Xu Qing
Zhang Han-Xiang
Lu Da-Bing
author_facet Liu Ze-Ting
Peng Han-Qi
Qi Yu-Xin
Wu Xiao-Yan
Xu Qing
Zhang Han-Xiang
Lu Da-Bing
author_sort Liu Ze-Ting
collection DOAJ
description China was once a major endemic zone for Schistosoma japonicum, but decades of control efforts have dramatically reduced transmission. Suzhou City, in Jiangsu Province, a former hyperendemic area, achieved transmission interruption in 1995. However, the intermediate host Oncomelania hupensis persists and new habitats in non-endemic villages pose resurgence risks if parasites are reintroduced. To evaluate genetic resilience and dispersal potential, we analyzed six O. hupensis populations (214 snails) from ecologically distinct habitats in Wuzhong district, Suzhou (2018 to 2021): Guangfu (GF20 and GF21: wetlands), Jinting (JT18, JT19, and JT20: isolated island), and Dongshan (DS19: lakeside hills). Using nine microsatellite loci, we identified 91 alleles and assessed genetic diversity, structure, and demography. All populations exhibited low observed heterozygosity (Ho < 0.5), with bottlenecks detected in GF21, GF20, and JT20. Paradoxically, infinite effective population sizes (Ne) at 95% CI upper limits suggested retained adaptive potential. Significant genetic differentiation (FST = 0.287, p < 0.01) reflected habitat-driven isolation: Jinting’s island populations diverged markedly from Dongshan and Guangfu, while bidirectional gene flow (Nm > 1) between Guangfu’s temporally sampled populations indicated sustained genetic connectivity over time. DIYABC modeling traced JT20’s ancestry to admixture between Jinting (JT18) and Guangfu (GF20) sources, implicating flood-mediated dispersal. Despite local control efficacy, snails retain resilience via large Ne. These findings mandate habitat-tailored strategies: habitat modification and intensified molluscicide campaigns in Guangfu and targeted eradication of Jinting’s isolated populations. Integrating genetic surveillance into snail monitoring programs will be critical to sustaining transmission interruption and achieving elimination in ecologically complex regions.
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spelling doaj-art-a915c13dd89c475886f4897d8d3f87df2025-08-20T03:27:44ZengEDP SciencesParasite1776-10422025-01-01323810.1051/parasite/2025031parasite250009Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 yearsLiu Ze-Ting0Peng Han-Qi1Qi Yu-Xin2Wu Xiao-Yan3Xu Qing4Zhang Han-Xiang5Lu Da-Bing6https://orcid.org/0000-0002-6396-9033Department of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityDepartment of Epidemiology and Statistics, School of Public Health, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Medical College of Soochow UniversityChina was once a major endemic zone for Schistosoma japonicum, but decades of control efforts have dramatically reduced transmission. Suzhou City, in Jiangsu Province, a former hyperendemic area, achieved transmission interruption in 1995. However, the intermediate host Oncomelania hupensis persists and new habitats in non-endemic villages pose resurgence risks if parasites are reintroduced. To evaluate genetic resilience and dispersal potential, we analyzed six O. hupensis populations (214 snails) from ecologically distinct habitats in Wuzhong district, Suzhou (2018 to 2021): Guangfu (GF20 and GF21: wetlands), Jinting (JT18, JT19, and JT20: isolated island), and Dongshan (DS19: lakeside hills). Using nine microsatellite loci, we identified 91 alleles and assessed genetic diversity, structure, and demography. All populations exhibited low observed heterozygosity (Ho < 0.5), with bottlenecks detected in GF21, GF20, and JT20. Paradoxically, infinite effective population sizes (Ne) at 95% CI upper limits suggested retained adaptive potential. Significant genetic differentiation (FST = 0.287, p < 0.01) reflected habitat-driven isolation: Jinting’s island populations diverged markedly from Dongshan and Guangfu, while bidirectional gene flow (Nm > 1) between Guangfu’s temporally sampled populations indicated sustained genetic connectivity over time. DIYABC modeling traced JT20’s ancestry to admixture between Jinting (JT18) and Guangfu (GF20) sources, implicating flood-mediated dispersal. Despite local control efficacy, snails retain resilience via large Ne. These findings mandate habitat-tailored strategies: habitat modification and intensified molluscicide campaigns in Guangfu and targeted eradication of Jinting’s isolated populations. Integrating genetic surveillance into snail monitoring programs will be critical to sustaining transmission interruption and achieving elimination in ecologically complex regions.https://www.parasite-journal.org/articles/parasite/full_html/2025/01/parasite250009/parasite250009.htmloncomelania hupensispopulation genetic analysesmicrosatellitessnail monitoring
spellingShingle Liu Ze-Ting
Peng Han-Qi
Qi Yu-Xin
Wu Xiao-Yan
Xu Qing
Zhang Han-Xiang
Lu Da-Bing
Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
Parasite
oncomelania hupensis
population genetic analyses
microsatellites
snail monitoring
title Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
title_full Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
title_fullStr Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
title_full_unstemmed Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
title_short Genetic diversity and structure of Oncomelania hupensis snails in an area where Schistosoma japonicum transmission has been interrupted for nearly 30 years
title_sort genetic diversity and structure of oncomelania hupensis snails in an area where schistosoma japonicum transmission has been interrupted for nearly 30 years
topic oncomelania hupensis
population genetic analyses
microsatellites
snail monitoring
url https://www.parasite-journal.org/articles/parasite/full_html/2025/01/parasite250009/parasite250009.html
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