ECOLOGICAL ASPECTS OF HOST-PARASITE COEVOLUTION AND THEIR IMPLICATIONS IN THE GENETIC CONTROL OF SCHISTOSOMIASIS

DENNIS JAMES MINCHELLA, Purdue University

Abstract

Schistosomiasis, a disease caused by a parasitic blood fluke, is a major health problem in more than seventy countries in Asia, Africa, the Caribbean and Latin America. The schistosome parasites responsible for human disease develop in a complicated life cycle involving freshwater snails. Schistosomiasis control has centered around the elimination of snail hosts, but this has not been very effective. A method of interrupting the life cycle of the schistosomes by increasing the proportion of genetically resistant snails in the natural population has been proposed. The method assumes that snails infected by the schistosome parasite suffer a loss in reproductive success compared to uninfected susceptible and resistant snails. Therefore resistant snails should be at a selective advantage in the presence of the parasite, and the technique proposes that natural selection will act to increase the proportion of alleles for resistance. A major objection to the proposed genetic control technique and the central issue addressed in this thesis is "If resistant snails are at a selective advantage, then why are they not predominant in natural populations that transmit disease?" Estimates of reproductive success of resistant and susceptible stocks of Biomphalaria glabrata tested individually or in combination, and in the presence of Schistosoma mansoni were used in order to determine whether a negative genetic correlation exists between resistance and other characters affecting reproductive success such as fecundity or competitive ability which puts resistant snails at a selective disadvantage. Results show that resistant snails are at a selective disadvantage when in the presence of susceptible snails, even in the presence of the parasite. If this result is generally applicable and resistant snails are selectively disadvantaged, then this provides a potentially simple explanation of why resistant snails do not predominate natural populations. Biomphalaria glabrata and B. alexandrina snails exposed to their coevolved strain of S. mansoni compensate, in part, for expected future loss in reproductive success through an increase in egg-laying during the pre-patent period. Early reproduction through fecundity compensation may increase reproductive success significantly especially in an expanding snail population. This life history adaptation may help parasitized hosts temper the impact of schistosome infection and may further explain why resistant snails do not predominate natural populations. Thus resistant snails are at a selective disadvantage in the presence of susceptible snails and therefore natural selection will not derive the proposed genetic control scheme. Even if resistant snails were not disadvantaged snail adaptations like fecundity compensation may help keep resistant snails from becoming predominant. Other mechanisms that may also play a role in maintaining genetic heterogeneity in snail susceptibility include spatial and temporal variation in parasite pressure, frequency-dependent selection, genetic drift, and host-parasite coevolution. Therefore the data herein demonstrate that natural selection will not act to increase the proportion of alleles for resistance. A major perturbation of the snail population through the influx of large numbers of resistant snails may reduce human disease locally for a short time. However, the host-parasite system must be closely monitored as parasite coevolutionary changes should be expected if the perturbation is not substantial.

Degree

Ph.D.

Subject Area

Ecology

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