Schistosoma mansoni: Relationship between cercarial production levels and snail host susceptibility

Ward, Rita D.; Lewis, Fred A.; Yoshino, Timothy P.; Dunn, Terry S.

doi:10.1016/0014-4894(88)90052-5

Cited by 25 publications

(10 citation statements)

References 17 publications

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“…An alternative explanation is that virulence may be a result of poor compatibility between host and parasite. Compatibility is measured as the ability of the schistosomes to infect intermediate host snails successfully and high compatibility in both laboratory and ¢eld populations is characterized by a high frequency of patent infections, high levels of cercarial production and low host mortality (Barbosa 1975;Ward et al 1988). Although much still needs to be understood about the precise mechanisms involved, it appears that, in compatible interactions, the snail does not launch an e¡ec-tive defensive response and parasites successfully establish and develop (Richards et al 1992).…”

Section: Discussionmentioning

confidence: 99%

Trade–offs in the evolution of virulence in an indirectly transmitted macroparasite

Davies

Webster

Woolhouse

2001

Proc. R. Soc. Lond. B

103

107

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The adaptive trade-o¡ theory for the evolution and maintenance of parasite virulence requires that virulence be genetically correlated with other ¢tness characteristics of the parasite. Many theoretical models rely on a positive correlation between virulence and transmissibility. They assume that high parasite replication rates are associated with a high probability of transmission (and, hence, increased parasite ¢tness), but also with high levels of damage to the host (high virulence). Schistosomes are macroparasites with an indirect life cycle involving a mammalian and a molluscan host. Here we demonstrate, through the development of ¢ve substrains, a genetic basis for schistosome virulence. We used these substrains further in order to investigate the presence of parasite ¢tness traits that were genetically correlated with virulence. High virulence in the (mouse) de¢nitive host was, as predicted, positively correlated with parasite replication. In contrast, in the (snail) intermediate host high virulence was associated with low parasite replication rates. Variation in infectivity to and parasite replication in the de¢nitive host was suggested as a compensating mechanism for the maintenance of virulence in the snail host. This is the ¢rst report of a trade-o¡ in parasite reproductive success across hosts in an indirectly transmitted macroparasite.

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Section: Discussionmentioning

confidence: 99%

Trade–offs in the evolution of virulence in an indirectly transmitted macroparasite

Davies

Webster

Woolhouse

2001

Proc. R. Soc. Lond. B

103

107

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“…Snails are often abundant and difficult to control, and it is in snails that the cercariae infective to humans are produced in prolific numbers. It takes only a single schistosome miracidium to establish a snail infection capable of producing hundreds of cercariae on a daily basis for months [2]. The amplification of schistosomes that occurs within snails creates a reoccurring problem for control efforts and is a significant obstacle for sustained prevention.…”

Section: Introductionmentioning

confidence: 99%

A Somatically Diversified Defense Factor, FREP3, Is a Determinant of Snail Resistance to Schistosome Infection

2012

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Schistosomiasis, a neglected tropical disease, owes its continued success to freshwater snails that support production of prolific numbers of human-infective cercariae. Encounters between schistosomes and snails do not always result in the snail becoming infected, in part because snails can mount immune responses that prevent schistosome development. Fibrinogen-related protein 3 (FREP3) has been previously associated with snail defense against digenetic trematode infection. It is a member of a large family of immune molecules with a unique structure consisting of one or two immunoglobulin superfamily domains connected to a fibrinogen domain; to date fibrinogen containing proteins with this arrangement are found only in gastropod molluscs. Furthermore, specific gastropod FREPs have been shown to undergo somatic diversification. Here we demonstrate that siRNA mediated knockdown of FREP3 results in a phenotypic loss of resistance to Schistosoma mansoni infection in 15 of 70 (21.4%) snails of the resistant BS-90 strain of Biomphalaria glabrata. In contrast, none of the 64 control BS-90 snails receiving a GFP siRNA construct and then exposed to S. mansoni became infected. Furthermore, resistance to S. mansoni was overcome in 22 of 48 snails (46%) by pre-exposure to another digenetic trematode, Echinostoma paraensei. Loss of resistance in this case was shown by microarray analysis to be associated with strong down-regulation of FREP3, and other candidate immune molecules. Although many factors are certainly involved in snail defense from trematode infection, this study identifies for the first time the involvement of a specific snail gene, FREP3, in the phenotype of resistance to the medically important parasite, S. mansoni. The results have implications for revealing the underlying mechanisms involved in dictating the range of snail strains used by S. mansoni, and, more generally, for better understanding the phenomena of host specificity and host switching. It also highlights the role of a diversified invertebrate immune molecule in defense against a human pathogen. It suggests new lines of investigation for understanding how susceptibility of snails in areas endemic for S. mansoni could be manipulated and diminished.

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“…The pro®le of cercarial emergence from P. marmorata and L. columella for two infective doses indicates that it was probably in¯uenced by E. paraensei (Ward et al 1988). However, L. columella always released the highest (Kanev 1994) number of cercariae when compared with the other two species tested and had a higher mortality rate.…”

Section: Discussionmentioning

confidence: 99%

Biological aspects of a new isolate of Echinostoma paraensei (Trematoda: Echinostomatidae): susceptibility of sympatric snails and the natural vertebrate host

Maldonado

et al. 2001

Parasitology Research

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A new isolate of Echinostoma paraensei (Lie & Basch, 1967) was obtained from a natural vertebrate host, the water rat Nectomys squamipes. Relationships with sympatric snails, Biomphalaria glabrata; Physa marmorata and Lymnaea columella, as well as allopatric snails and the definitive hosts N. squamipes, Mus musculus, Rattus norvegicus, Mesocricetus auratus and birds were investigated. E. paraensei developed in all sympatric snail species following exposure to one or five miracidia. P. marmorata showed the highest infection rate (34% and 36%) followed by L. columella (18% and 24%) and B. glabrata (8% and 28%), respectively. Mortality was elevated in the patent period, with L. columella having the highest values. B. glabrata, P. marmorata, and L. columella did not differ in relation to cercarial encystment, and metacercariae from each species were able to infect N. squamipes with similar worm burdens. Recovered adult worms were found in clusters from the first to third sections of the small intestine. Miracidia of E. paraensei hatched after 10 days incubation in darkness in dechlorinated water at 28+/-1 micro C. Miracidia began to hatch 1 h after exposure to incandescent light.

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Schistosoma mansoni: Relationship between cercarial production levels and snail host susceptibility

Cited by 25 publications

References 17 publications

Trade–offs in the evolution of virulence in an indirectly transmitted macroparasite

Trade–offs in the evolution of virulence in an indirectly transmitted macroparasite

A Somatically Diversified Defense Factor, FREP3, Is a Determinant of Snail Resistance to Schistosome Infection

Biological aspects of a new isolate of Echinostoma paraensei (Trematoda: Echinostomatidae): susceptibility of sympatric snails and the natural vertebrate host

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