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Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations
BACKGROUND: Parasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait, i.e. the number of cercariae larvae sh...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796389/ https://www.ncbi.nlm.nih.gov/pubmed/31619284 http://dx.doi.org/10.1186/s13071-019-3741-z |
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author | Le Clecʼh, Winka Diaz, Robbie Chevalier, Frédéric D. McDew-White, Marina Anderson, Timothy J. C. |
author_facet | Le Clecʼh, Winka Diaz, Robbie Chevalier, Frédéric D. McDew-White, Marina Anderson, Timothy J. C. |
author_sort | Le Clecʼh, Winka |
collection | PubMed |
description | BACKGROUND: Parasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait, i.e. the number of cercariae larvae shed from infected Biomphalaria spp. snails, varies significantly within and between different parasite populations and selection experiments demonstrate that this variation has a strong genetic basis. In this study, we compared the transmission strategies of two laboratory schistosome population and their consequences for their snail host. METHODS: We infected inbred Biomphalaria glabrata snails using two S. mansoni parasite populations (SmBRE and SmLE), both isolated from Brazil and maintained in the laboratory for decades. We compared life history traits of these two parasite populations by quantifying sporocyst growth within infected snails (assayed using qPCR), output of cercaria larvae and impact on snail host physiological response (i.e. hemoglobin rate, laccase-like activity) and survival. RESULTS: We identified striking differences in virulence and transmission between the two studied parasite populations. SmBRE (low shedder (LS) parasite population) sheds very low numbers of cercariae and causes minimal impact on the snail physiological response (i.e. laccase-like activity, hemoglobin rate and snail survival). In contrast, SmLE (high shedder (HS) parasite population) sheds 8-fold more cercariae (mean ± SE cercariae per shedding: 284 ± 19 vs 2352 ± 113), causes high snail mortality and has strong impact on snail physiology. We found that HS sporocysts grow more rapidly inside the snail host, comprising up to 60% of cells within infected snails, compared to LS sporocysts, which comprised up to 31%. Cercarial production is strongly correlated to the number of S. mansoni sporocyst cells present within the snail host tissue, although the proportion of sporocyst cells alone does not explain the low cercarial shedding of SmBRE. CONCLUSIONS: We demonstrated the existence of alternative transmission strategies in the S. mansoni parasite consistent with trade-offs between parasite transmission and host survival: a “boom-bust” strategy characterized by high virulence, high transmission and short duration infections and a “slow and steady” strategy with low virulence, low transmission but long duration of snail host infections. [Image: see text] |
format | Online Article Text |
id | pubmed-6796389 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-67963892019-10-21 Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations Le Clecʼh, Winka Diaz, Robbie Chevalier, Frédéric D. McDew-White, Marina Anderson, Timothy J. C. Parasit Vectors Research BACKGROUND: Parasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait, i.e. the number of cercariae larvae shed from infected Biomphalaria spp. snails, varies significantly within and between different parasite populations and selection experiments demonstrate that this variation has a strong genetic basis. In this study, we compared the transmission strategies of two laboratory schistosome population and their consequences for their snail host. METHODS: We infected inbred Biomphalaria glabrata snails using two S. mansoni parasite populations (SmBRE and SmLE), both isolated from Brazil and maintained in the laboratory for decades. We compared life history traits of these two parasite populations by quantifying sporocyst growth within infected snails (assayed using qPCR), output of cercaria larvae and impact on snail host physiological response (i.e. hemoglobin rate, laccase-like activity) and survival. RESULTS: We identified striking differences in virulence and transmission between the two studied parasite populations. SmBRE (low shedder (LS) parasite population) sheds very low numbers of cercariae and causes minimal impact on the snail physiological response (i.e. laccase-like activity, hemoglobin rate and snail survival). In contrast, SmLE (high shedder (HS) parasite population) sheds 8-fold more cercariae (mean ± SE cercariae per shedding: 284 ± 19 vs 2352 ± 113), causes high snail mortality and has strong impact on snail physiology. We found that HS sporocysts grow more rapidly inside the snail host, comprising up to 60% of cells within infected snails, compared to LS sporocysts, which comprised up to 31%. Cercarial production is strongly correlated to the number of S. mansoni sporocyst cells present within the snail host tissue, although the proportion of sporocyst cells alone does not explain the low cercarial shedding of SmBRE. CONCLUSIONS: We demonstrated the existence of alternative transmission strategies in the S. mansoni parasite consistent with trade-offs between parasite transmission and host survival: a “boom-bust” strategy characterized by high virulence, high transmission and short duration infections and a “slow and steady” strategy with low virulence, low transmission but long duration of snail host infections. [Image: see text] BioMed Central 2019-10-16 /pmc/articles/PMC6796389/ /pubmed/31619284 http://dx.doi.org/10.1186/s13071-019-3741-z Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Le Clecʼh, Winka Diaz, Robbie Chevalier, Frédéric D. McDew-White, Marina Anderson, Timothy J. C. Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title | Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title_full | Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title_fullStr | Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title_full_unstemmed | Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title_short | Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
title_sort | striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796389/ https://www.ncbi.nlm.nih.gov/pubmed/31619284 http://dx.doi.org/10.1186/s13071-019-3741-z |
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