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Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)

BACKGROUND: Gastropod snails remain strongly understudied, despite their important role in transmitting parasitic diseases. Knowledge of their distribution and population dynamics increases our understanding of the processes driving disease transmission. We report the first study to use high-through...

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Autores principales: Maes, Tim, De Corte, Zoë, Vangestel, Carl, Virgilio, Massimiliano, Smitz, Nathalie, Djuikwo-Teukeng, Félicité F., Papadaki, Maria Ioanna, Huyse, Tine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9484234/
https://www.ncbi.nlm.nih.gov/pubmed/36123605
http://dx.doi.org/10.1186/s13071-022-05445-x
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author Maes, Tim
De Corte, Zoë
Vangestel, Carl
Virgilio, Massimiliano
Smitz, Nathalie
Djuikwo-Teukeng, Félicité F.
Papadaki, Maria Ioanna
Huyse, Tine
author_facet Maes, Tim
De Corte, Zoë
Vangestel, Carl
Virgilio, Massimiliano
Smitz, Nathalie
Djuikwo-Teukeng, Félicité F.
Papadaki, Maria Ioanna
Huyse, Tine
author_sort Maes, Tim
collection PubMed
description BACKGROUND: Gastropod snails remain strongly understudied, despite their important role in transmitting parasitic diseases. Knowledge of their distribution and population dynamics increases our understanding of the processes driving disease transmission. We report the first study to use high-throughput sequencing (HTS) to elucidate the population genetic structure of the hermaphroditic snail Bulinus truncatus (Gastropoda, Heterobranchia) on a regional (17–150 km) and inter-regional (1000–5400 km) scale. This snail species acts as an intermediate host of Schistosoma haematobium and Schistosoma bovis, which cause human and animal schistosomiasis respectively. METHODS: Bulinus truncatus snails were collected in Senegal, Cameroon, Egypt and France and identified through DNA barcoding. A single-end genotyping-by-sequencing (GBS) library, comprising 87 snail specimens from the respective countries, was built and sequenced on an Illumina HiSeq 2000 platform. Reads were mapped against S. bovis and S. haematobium reference genomes to identify schistosome infections, and single nucleotide polymorphisms (SNPs) were scored using the Stacks pipeline. These SNPs were used to estimate genetic diversity, assess population structure and construct phylogenetic trees of B. truncatus. RESULTS: A total of 10,750 SNPs were scored and used in downstream analyses. The phylogenetic analysis identified five clades, each consisting of snails from a single country but with two distinct clades within Senegal. Genetic diversity was low in all populations, reflecting high selfing rates, but varied between locations due to habitat variability. Significant genetic differentiation and isolation by distance patterns were observed at both spatial scales, indicating that gene flow is not strong enough to counteract the effects of population bottlenecks, high selfing rates and genetic drift. Remarkably, the population genetic differentiation on a regional scale (i.e. within Senegal) was as large as that between populations on an inter-regional scale. The blind GBS technique was able to pick up parasite DNA in snail tissue, demonstrating the potential of HTS techniques to further elucidate the role of snail species in parasite transmission. CONCLUSIONS: HTS techniques offer a valuable toolbox to further investigate the population genetic patterns of intermediate schistosome host snails and the role of snail species in parasite transmission. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05445-x.
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spelling pubmed-94842342022-09-20 Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia) Maes, Tim De Corte, Zoë Vangestel, Carl Virgilio, Massimiliano Smitz, Nathalie Djuikwo-Teukeng, Félicité F. Papadaki, Maria Ioanna Huyse, Tine Parasit Vectors Research BACKGROUND: Gastropod snails remain strongly understudied, despite their important role in transmitting parasitic diseases. Knowledge of their distribution and population dynamics increases our understanding of the processes driving disease transmission. We report the first study to use high-throughput sequencing (HTS) to elucidate the population genetic structure of the hermaphroditic snail Bulinus truncatus (Gastropoda, Heterobranchia) on a regional (17–150 km) and inter-regional (1000–5400 km) scale. This snail species acts as an intermediate host of Schistosoma haematobium and Schistosoma bovis, which cause human and animal schistosomiasis respectively. METHODS: Bulinus truncatus snails were collected in Senegal, Cameroon, Egypt and France and identified through DNA barcoding. A single-end genotyping-by-sequencing (GBS) library, comprising 87 snail specimens from the respective countries, was built and sequenced on an Illumina HiSeq 2000 platform. Reads were mapped against S. bovis and S. haematobium reference genomes to identify schistosome infections, and single nucleotide polymorphisms (SNPs) were scored using the Stacks pipeline. These SNPs were used to estimate genetic diversity, assess population structure and construct phylogenetic trees of B. truncatus. RESULTS: A total of 10,750 SNPs were scored and used in downstream analyses. The phylogenetic analysis identified five clades, each consisting of snails from a single country but with two distinct clades within Senegal. Genetic diversity was low in all populations, reflecting high selfing rates, but varied between locations due to habitat variability. Significant genetic differentiation and isolation by distance patterns were observed at both spatial scales, indicating that gene flow is not strong enough to counteract the effects of population bottlenecks, high selfing rates and genetic drift. Remarkably, the population genetic differentiation on a regional scale (i.e. within Senegal) was as large as that between populations on an inter-regional scale. The blind GBS technique was able to pick up parasite DNA in snail tissue, demonstrating the potential of HTS techniques to further elucidate the role of snail species in parasite transmission. CONCLUSIONS: HTS techniques offer a valuable toolbox to further investigate the population genetic patterns of intermediate schistosome host snails and the role of snail species in parasite transmission. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05445-x. BioMed Central 2022-09-19 /pmc/articles/PMC9484234/ /pubmed/36123605 http://dx.doi.org/10.1186/s13071-022-05445-x 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
Maes, Tim
De Corte, Zoë
Vangestel, Carl
Virgilio, Massimiliano
Smitz, Nathalie
Djuikwo-Teukeng, Félicité F.
Papadaki, Maria Ioanna
Huyse, Tine
Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title_full Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title_fullStr Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title_full_unstemmed Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title_short Large-scale and small-scale population genetic structure of the medically important gastropod species Bulinus truncatus (Gastropoda, Heterobranchia)
title_sort large-scale and small-scale population genetic structure of the medically important gastropod species bulinus truncatus (gastropoda, heterobranchia)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9484234/
https://www.ncbi.nlm.nih.gov/pubmed/36123605
http://dx.doi.org/10.1186/s13071-022-05445-x
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