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Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China

BACKGROUND: Snail control is critical to schistosomiasis control efforts in China. However, re-emergence of Oncomelania hupensis is challenging the achievements of schistosomiasis control. The present study aimed to test whether the amphibious snails can spread across watersheds using a combination...

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Autores principales: Chen, Shen, Lu, Ding, Duan, Lei, Ma, Ben, Lv, Chao, Li, Yin-long, Lu, Shen-ning, Li, Lan-hua, Xu, Liang, Wu, Zi-song, Xia, Shang, Xu, Jing, Liu, Yang, Lv, Shan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9555091/
https://www.ncbi.nlm.nih.gov/pubmed/36221118
http://dx.doi.org/10.1186/s13071-022-05496-0
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author Chen, Shen
Lu, Ding
Duan, Lei
Ma, Ben
Lv, Chao
Li, Yin-long
Lu, Shen-ning
Li, Lan-hua
Xu, Liang
Wu, Zi-song
Xia, Shang
Xu, Jing
Liu, Yang
Lv, Shan
author_facet Chen, Shen
Lu, Ding
Duan, Lei
Ma, Ben
Lv, Chao
Li, Yin-long
Lu, Shen-ning
Li, Lan-hua
Xu, Liang
Wu, Zi-song
Xia, Shang
Xu, Jing
Liu, Yang
Lv, Shan
author_sort Chen, Shen
collection PubMed
description BACKGROUND: Snail control is critical to schistosomiasis control efforts in China. However, re-emergence of Oncomelania hupensis is challenging the achievements of schistosomiasis control. The present study aimed to test whether the amphibious snails can spread across watersheds using a combination of population genetics and geographic statistics. METHODS: The digital maps and attributes of snail habitats were obtained from the national survey on O. hupensis. Snail sampling was performed in 45 counties of Sichuan Province. The cox1 gene of specimens was characterized by sequencing. Unique haplotypes were found for phylogenetic inference and mapped in a geographical information system (GIS). Barriers of gene flow were identified by Monmonier’s maximum difference algorithm. The watercourses and watersheds in the study area were determined based on a digital elevation model (DEM). Plain areas were defined by a threshold of slope. The slope of snail habitats was characterized and the nearest distance to watercourses was calculated using a GIS platform. Spatial dynamics of high-density distributions were observed by density analysis of snail habitats. RESULTS: A total of 422 cox1 sequences of O. hupensis specimens from 45 sampling sites were obtained and collapsed into 128 unique haplotypes or 10 clades. Higher haplotype diversity in the north of the study area was observed. Four barriers to gene flow, leading to five sub-regions, were found across the study area. Four sub-regions ran across major watersheds, while high-density distributions were confined within watersheds. The result indicated that snails were able to disperse across low-density areas. A total of 63.48% habitats or 43.29% accumulated infested areas were distributed in the plain areas where the overall slope was < 0.94°. Approximately 90% of snail habitats were closer to smaller watercourses. Historically, high-density areas were mainly located in the plains, but now more were distributed in hilly region. CONCLUSIONS: Our study showed the cross-watershed distribution of Oncomelania snails at a large scale. Natural cross-watershed spread in plains and long-distance dispersal by humans and animals might be the main driver of the observed patterns. We recommend cross-watershed joint control strategies for snail and schistosomiasis control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05496-0.
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spelling pubmed-95550912022-10-13 Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China Chen, Shen Lu, Ding Duan, Lei Ma, Ben Lv, Chao Li, Yin-long Lu, Shen-ning Li, Lan-hua Xu, Liang Wu, Zi-song Xia, Shang Xu, Jing Liu, Yang Lv, Shan Parasit Vectors Research BACKGROUND: Snail control is critical to schistosomiasis control efforts in China. However, re-emergence of Oncomelania hupensis is challenging the achievements of schistosomiasis control. The present study aimed to test whether the amphibious snails can spread across watersheds using a combination of population genetics and geographic statistics. METHODS: The digital maps and attributes of snail habitats were obtained from the national survey on O. hupensis. Snail sampling was performed in 45 counties of Sichuan Province. The cox1 gene of specimens was characterized by sequencing. Unique haplotypes were found for phylogenetic inference and mapped in a geographical information system (GIS). Barriers of gene flow were identified by Monmonier’s maximum difference algorithm. The watercourses and watersheds in the study area were determined based on a digital elevation model (DEM). Plain areas were defined by a threshold of slope. The slope of snail habitats was characterized and the nearest distance to watercourses was calculated using a GIS platform. Spatial dynamics of high-density distributions were observed by density analysis of snail habitats. RESULTS: A total of 422 cox1 sequences of O. hupensis specimens from 45 sampling sites were obtained and collapsed into 128 unique haplotypes or 10 clades. Higher haplotype diversity in the north of the study area was observed. Four barriers to gene flow, leading to five sub-regions, were found across the study area. Four sub-regions ran across major watersheds, while high-density distributions were confined within watersheds. The result indicated that snails were able to disperse across low-density areas. A total of 63.48% habitats or 43.29% accumulated infested areas were distributed in the plain areas where the overall slope was < 0.94°. Approximately 90% of snail habitats were closer to smaller watercourses. Historically, high-density areas were mainly located in the plains, but now more were distributed in hilly region. CONCLUSIONS: Our study showed the cross-watershed distribution of Oncomelania snails at a large scale. Natural cross-watershed spread in plains and long-distance dispersal by humans and animals might be the main driver of the observed patterns. We recommend cross-watershed joint control strategies for snail and schistosomiasis control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05496-0. BioMed Central 2022-10-11 /pmc/articles/PMC9555091/ /pubmed/36221118 http://dx.doi.org/10.1186/s13071-022-05496-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Chen, Shen
Lu, Ding
Duan, Lei
Ma, Ben
Lv, Chao
Li, Yin-long
Lu, Shen-ning
Li, Lan-hua
Xu, Liang
Wu, Zi-song
Xia, Shang
Xu, Jing
Liu, Yang
Lv, Shan
Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title_full Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title_fullStr Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title_full_unstemmed Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title_short Cross-watershed distribution pattern challenging the elimination of Oncomelania hupensis, the intermediate host of Schistosoma japonica, in Sichuan province, China
title_sort cross-watershed distribution pattern challenging the elimination of oncomelania hupensis, the intermediate host of schistosoma japonica, in sichuan province, china
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9555091/
https://www.ncbi.nlm.nih.gov/pubmed/36221118
http://dx.doi.org/10.1186/s13071-022-05496-0
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