Spatial parasite transmission, drug resistance, and the spread of rare genes

Abstract

The transmission of many parasitic worms involves aggregated movement between hosts of "packets" of infectious larvae. We use a generic metapopulation model to show that this aggregation naturally promotes the preferential spread of rare recessive genes, compared with the expectations of traditional nonspatial models. A more biologically realistic model also demonstrates that this effect could explain the rapid observed spread of recessive or weakly dominant drug-resistant genotypes in nematode parasites of sheep. This promotion of a recessive trait arises from a novel mechanism of inbreeding arising from the metapopulation dynamics of transmission.

Fig. 1.

Schema of the generic branching metapopulation model. Adult worms mate in the host and produce offspring, which pass out of the host in “clumps.” A clump can then infect another host.

Fig. 2.

Simulations of the generic model, with clumping parameter 2: prevalence of the rare homozygote as a function of allele frequency at different times. Lines with n_ss ∞ q and n_ss = q² and are included for comparison purposes.

Fig. 3.

Sheep–trichostrongylid model. (A) Schematic diagram. (B) Worms per host (in blue) and larvae per hectare (in red) for two typical realizations, one corresponding to extinction (dotted lines) and one to an epidemic (solid lines). (C) Invasion probability both with (inbred) and without (random) spatial inbreeding, for different values of the clumping parameter; the error bars are standard errors from the simulations (based on >10,000 realizations).