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Increased reproductive fitness of HS parasite line in rodents. (A) The ability of cercarial larvae to infect their rodent definitive host is similar for LS and HS lines, in both genetic crosses, as a comparable number of worms were recovered from mice infected with HS and LS parasites after being exposed to the same number of cercariae. (B) In both crosses, the HS parasite line produced significantly more live miracidia (recovered from rodent infected livers) compared to the LS parasites, and therefore (C) HS reproductive fitness (total number of miracidia recovered/total number of female worms) is higher than in LS parasites. NS: No significant difference between the considered groups; *P < 0.05; **P ≤ 0.01; ***P ≤ 0.001
Source publication
Background
The trematode parasite Schistosoma mansoni uses an aquatic snail intermediate and a vertebrate definitive host to complete its life cycle. We previously showed that a key transmission trait—the number of cercariae larvae shed from infected Biomphalaria spp. snails—varies significantly within and between different parasite populations and...
Citations
... Low or high shedding populations derived from crosses between these two parasite populations also varied in life history traits in the rodent host. Low shedding parasites showed lower fecundity, reduced hepatosplenomegaly and hepatic fibrosis in mice than high shedding parasites [19]. ...
... We maintain four distinct S. mansoni populations in our laboratory (SmEG from Egypt, SmLE and SmBRE from Brazil and SmOR, descended from the SmHR population [24] from Puerto Rico), which we used in this study. These parasite populations show distinctive phenotypes: SmLE shows eightfold higher cercarial production than SmBRE as well as larger sporocysts, higher infectivity to mice and higher fecundity [18,19]; SmOR is an oxamniquine resistant population homozygous for the deletion in amino acid 142 in SmSULT-OR [25]; SmEG is the only population with African origin. Our central aim was to investigate the impact of parasite genetics on immunopathology while accounting for host genetic differences. ...
... This is clearly shown by examining correlations between egg burden and organ weight (Additional file 6: Fig. S5). This study confirms and extends our previous findings from studies of two Brazilian populations, SmBRE and SmLE, that show striking differences in cercarial shedding and sporocyst growth in the intermediate snail host [18,19,53]. These two parasite populations also showed the most extreme phenotype differences during infection in the vertebrate host. ...
Background
The role of pathogen genotype in determining disease severity and immunopathology has been studied intensively in microbial pathogens including bacteria, fungi, protozoa and viruses but is poorly understood in parasitic helminths. The medically important blood fluke Schistosoma mansoni is an excellent model system to study the impact of helminth genetic variation on immunopathology. Our laboratory has demonstrated that laboratory schistosome populations differ in sporocyst growth and cercarial production in the intermediate snail host and worm establishment and fecundity in the vertebrate host. Here, we (i) investigate the hypothesis that schistosome genotype plays a significant role in immunopathology and related parasite life history traits in the vertebrate mouse host and (ii) quantify the relative impact of parasite and host genetics on infection outcomes.
Methods
We infected BALB/c and C57BL/6 mice with four different laboratory schistosome populations from Africa and the Americas. We quantified disease progression in the vertebrate host by measuring body weight and complete blood count (CBC) with differential over a 12-week infection period. On sacrifice, we assessed parasitological (egg and worm counts, fecundity), immunopathological (organ measurements and histopathology) and immunological (CBC with differential and cytokine profiles) characteristics to determine the impact of parasite and host genetics.
Results
We found significant variation between parasite populations in worm numbers, fecundity, liver and intestine egg counts, liver and spleen weight, and fibrotic area but not in granuloma size. Variation in organ weight was explained by egg burden and intrinsic parasite factors independent of egg burden. We found significant variation between infected mouse lines in cytokine levels (IFN-γ, TNF-α), eosinophils, lymphocytes and monocyte counts.
Conclusions
This study showed that both parasite and host genotype impact the outcome of infection. While host genotype explains most of the variation in immunological traits, parasite genotype explains most of the variation in parasitological traits, and both host and parasite genotypes impact immunopathology outcomes.
Graphical Abstract
... Low shedding parasites showed lower fecundity, reduced hepatosplenomegaly and hepatic brosis in mice than high shedding parasites [17]. ...
... This study con rms and extends our previous ndings from studies of two Brazilian populations, SmBRE and SmLE, that show striking differences in cercarial shedding and sporocyst growth in the intermediate snail host [16,17,47]. These two parasite populations also showed the most extreme phenotype differences during infection in the vertebrate host. ...
... Additionally, parameters such as liver weight, spleen weight, and brotic area were also lower in SmBRE-infected mice compared to the other schistosome populations characterized in the present study. We have previously demonstrated that brotic area and granuloma size were reduced in mice infected with parasite progeny from SmBRE and SmLE genetic crosses selected for low or high cercarial shedding from the aquatic snail [17]. While the experimental design in this study was rather different, we saw comparable differences in brotic area (lower in SmBRE than in SmLE), although granuloma size was unaffected. ...
Background
The role of pathogen genotype in determining disease severity and immunopathology has been studied intensively in microbial pathogens including bacteria, fungi, protozoa, and viruses, but is poorly understood in parasitic helminths. The medically important blood fluke Schistosoma mansoni is an excellent model system to study the impact of helminth genetic variation on immunopathology. Our laboratory has demonstrated that laboratory schistosome populations differ in sporocyst growth and cercarial production in the intermediate snail host and worm establishment and fecundity in the vertebrate host. Here, we (i) investigate the hypothesis that schistosome genotype plays a significant role in immunopathology and related parasite life history traits in the vertebrate mouse host and (ii) quantify the relative impact of parasite and host genetics on infection outcomes.
Methods
We infected BALB/c and C57BL/6 mice with four different laboratory schistosome populations from Africa and the Americas. We quantified disease progression in the vertebrate host by measuring body weight and complete blood count (CBC) with differential over an infection period of 12 weeks. On sacrifice, we assessed parasitological (egg and worm counts, fecundity), immunopathological (organ measurements and histopathology), and immunological (CBC with differential and cytokine profiles) characteristics to determine the impact of parasite and host genetics.
Results
We found significant variation between parasite populations in worm numbers, fecundity, liver and intestine egg counts, liver and spleen weight, and fibrotic area, but not in granuloma size. Variation in organ weight was explained by egg burden and by intrinsic parasite factors independent of egg burden. We found significant variation between infected mouse lines in cytokines (IFN-γ, TNF-α), eosinophil, lymphocyte, and monocyte counts.
Conclusions
This study showed that both parasite and host genotype impact the outcome of infection. While host genotype explains most of the variation in immunological traits, parasite genotype explains most of the variation in parasitological traits, and both host and parasite genotype impact immunopathology outcomes.
... Fast-developing genotypes, however, did not have reduced growth in sticklebacks or reduced fecundity in the in vitro bird. Similarly, experimental evolution of the ability of S. solidus to manipulate copepod behavior did not have correlated effects on plerocercoid growth or fecundity (Hafer-Hahmann 2019), which does not support cross-host tradeoffs (Le Clec'h et al. 2022). Perhaps shared genetic mechanisms are more likely for tasks, like invasion or growth, that parasites undertake in more than one host. ...
Evolutionary stasis characterizes many phenotypes, even ones that seem suboptimal. Among tapeworms, Schistocephalus solidus and its relatives have some of the shortest developmental times in their first intermediate hosts, yet their development still seems excessively long considering they can grow faster, larger, and safer in the next hosts in their complex life cycles. I conducted four generations of selection on the developmental rate of S. solidus in its copepod first host, pushing a conserved-but-counterintuitive phenotype towards the limit of known tapeworm life-history strategies. Faster parasite development evolved and enabled earlier infectivity to the stickleback next host, but low heritability for infectivity moderated fitness gains. Fitness losses were more pronounced for slow-developing parasite families, irrespective of selection line, because directional selection released linked genetic variation for reduced infectivity to copepods, developmental stability, and fecundity. This deleterious variation is normally suppressed, implying development is canalized and thus under stabilizing selection. Nevertheless, faster development was not costly; fast-developing genotypes did not decrease copepod survival, even under host starvation, nor did they underperform in the next hosts, suggesting parasite stages in successive hosts are genetically decoupled. I speculate that, on longer time scales, the ultimate cost of abbreviated development is reduced size-dependent infectivity.
