Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Abstract

BackgroundParasite 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 – 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.MethodsWe infected inbred Biomphalaria glabrata snails using two Schistosoma 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.ResultsWe 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.ConclusionsWe 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.

Population genetics of African Schistosoma species

“…a phenomenon called "compatibility") (Mitta et al, 2017;Theron et al, 2014). Interestingly, experimental comparative studies have shown adaptative trade-offsaccording to the parasite strain (Davies et al, 2001;Le Clec'h et al, 2019).…”

Genetic analysis of praziquantel response in schistosome parasites implicates a Transient Receptor Potential channel

“…We plated 120 SmLE-PZQ-R adult male worms individually in 96-well plates, treated them with PZQ (24.3 µg/mL) and collected media supernatants pre-(24 h) and post-(48 h) treatment, and used L-lactate assays to determine PZQ-R status. We extracted gDNA from each worm individually (66).…”

“…All snails used in this study had a shell diameter between 8 and 10 mm. We used inbred snails to minimize the impact of snail host genetic background on the parasite life history traits (66).…”

“…QTL genotype using the PCR-RFLP as described. We exposed 960 inbred B. glabrata Bg121 snails to one miracidium SmLE-PZQ-R (66). At four weeks post-exposure, we identified infected snail (N=272), and collected cercariae from individual snails.…”

“…Complementary DNA (cDNA) was generated from extracted RNA (500 ng -1 µg) using SuperScript-III and Oligo-dT primers (ThermoFisher). Relative quantification of genes of interest was performed in duplicate by qPCR analysis using QuantStudio 5 System (Applied Biosystems) and SYBR Green master mix (ThermoFisher), compared with a serially diluted standard of PCR products (generated from cDNA) for each of the gene tested (66). Standard curves allow evaluating the efficiency of each pairs of primers, for both housekeeping and target genes using QuantStudio Design and Analysis Software.…”