Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations
Abstract 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 l...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2019-10-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-019-3741-z |
| _version_ | 1819000933773737984 |
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| author | Winka Le Clecʼh Robbie Diaz Frédéric D. Chevalier Marina McDew-White Timothy J. C. Anderson |
| author_facet | Winka Le Clecʼh Robbie Diaz Frédéric D. Chevalier Marina McDew-White Timothy J. C. Anderson |
| author_sort | Winka Le Clecʼh |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-20T22:41:12Z |
| format | Article |
| id | doaj.art-2134c2ac88804132a6e02e3fa2d8dc8f |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-20T22:41:12Z |
| publishDate | 2019-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-2134c2ac88804132a6e02e3fa2d8dc8f2022-12-21T19:24:28ZengBMCParasites & Vectors1756-33052019-10-0112111210.1186/s13071-019-3741-zStriking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populationsWinka Le Clecʼh0Robbie Diaz1Frédéric D. Chevalier2Marina McDew-White3Timothy J. C. Anderson4Texas Biomedical Research InstituteTexas Biomedical Research InstituteTexas Biomedical Research InstituteTexas Biomedical Research InstituteTexas Biomedical Research InstituteAbstract 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.http://link.springer.com/article/10.1186/s13071-019-3741-zSchistosoma mansoniBiomphalaria glabrataLife-history traitsVirulenceTransmissionHemoglobin rate |
| spellingShingle | Winka Le Clecʼh Robbie Diaz Frédéric D. Chevalier Marina McDew-White Timothy J. C. Anderson Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations Parasites & Vectors Schistosoma mansoni Biomphalaria glabrata Life-history traits Virulence Transmission Hemoglobin rate |
| 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 | Schistosoma mansoni Biomphalaria glabrata Life-history traits Virulence Transmission Hemoglobin rate |
| url | http://link.springer.com/article/10.1186/s13071-019-3741-z |
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