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, 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.MethodsWe 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.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.
Highlights
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
Models predicting the evolution of virulence for parasites transmitted horizontally assume generally that transmission rate and virulence are positively correlated, as higher production of infective stages may be more harmful for the host [1,2,3,4]
All the infected snails were from the same inbred B. glabrata population (Bg26) to minimize the impact of the host genetic background, because we know that cercarial shedding can be influenced by the snail genotype [29]
Summary
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. For most of the virulence evolution models, such a trade-off shapes the relationship between parasite transmission and host survival (the higher the virulence of the parasite, the shorter the host survival and in turn the parasite lifespan) [5] for both micro- [6] and macroparasites [7]. Larvae penetrate the snail head–foot, differentiate into mother sporocysts and asexually proliferate to generate daughter sporocysts This intramolluscan parasite stages feed on snail tissues such as the hepatopancreas and the albumen gland [10,11,12]. After approximately a month of infection, daughter sporocysts start to release cercariae, the mammal infective larval stage of the parasite These exit through the snail body wall and are released into the water. This complex life-cycle can be maintained in the laboratory using rodent definitive hosts and freshwater snail intermediate hosts
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