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 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.

Chlorination of Schistosoma mansoni cercariae

“…Growth condition can change a microorganism’s chlorine resistance by altering the cell envelope [ 10 ], which is especially the case for bacteria. The growth condition is known to significantly affect a snail’s cercarial production [ 23 , 24 ], but it is unknown if it also affects the morphology and physiology of cercariae. Cercariae are non-feeding and may therefore be less affected by the water composition compared to other microorganisms that depend on the water matrix as a growth medium.…”

Genetic architecture of transmission stage production and virulence in schistosome parasites

“…Difference in the average of cercariae produced by SmLE-H and SmBRE-L S. mansoni populations during 4 weeks of the patent period (week 4 to 7 post infection). SmLE-H population is shedding more cercariae than SmBRE-L population (Le Clecʼh et al, 2019). For both crosses A and B, F1s populations exhibit intermediate phenotype in terms of cercarial production, compared to F0, while the average production of cercariae by F2s encompass both parental and F1s distributions.…”

“…Schistosomes are sex separated parasites that simplifies crosses (Valentim et al, 2013). In order to identify QTL(s) controlling the number of cercariae produced by schistosome parasites, we conducted crosses between parasites from our high shedder (SmLE-H) and low shedder (SmBRE-L) populations (Le Clecʼh et al, 2019). We performed two reciprocal genetic crosses (cross A: male SmBRE (L) x female SmLE (H); cross B: female SmBRE (L) x male SmLE (H)) to i) replicate our cross experiment and ii) to test for the potential influence of sex chromosomes on the transmission phenotype (Figure 1).…”

“…Larvae penetrate the snail head-foot, differentiate into sporocysts that then asexually proliferate to generate daughter sporocysts. These actively consume snail tissue (hepatopancreas and ovotestis), castrating the host snail, and parasite sporocysts can comprise up to 60% of the tissue within infected snails (Le Clecʼh et al, 2019). The daughter sporocysts release cercariae, the mammal-infective larval stage of the parasite.…”

“…impact of schistosome infection (LeLe Clecʼh et al, 2019). Both parameters were negatively correlated with F2 cercarial production (laccase-like activity: Pearson's correlation test, p = 4.31 × 10 -15 , correlation coefficient = -0.56; Hemoglobin rate: Pearson's correlation test, p = 8.014 × 10 -12 , correlation coefficient = -0.50; Supplementary figure 3D and 3E).…”