Nematodes are a major cause of disease and death in humans, domestic animals and wildlife. Understanding why some individuals suffer severely whereas others exposed to the same infection remain healthy may assist in the development of rational and sustainable strategies to control infection. Here, using a quantitative genetic analysis of the parasitic nematode population that had accumulated naturally in lambs, we find no apparent influence of host genetics on nematode numbers but an extremely strong influence on average worm length and fecundity. Our results indicate that in growing lambs the main manifestation of genetic resistance is the control of worm fecundity.

The lambs were all straight-bred Scottish blackface sheep from a commercial farm in southwest Strathclyde. We took faecal samples from the rectum of each lamb in late May when the lambs were 3-5 weeks old and then at four-week intervals. After taking each sample, animals were treated with a broad-spectrum anthelmintic (albendazole sulphoxide; Rycoben, Youngs Animal Health, Leyland, UK), given at the recommended dose rate of 5 mg per kg body mass. We assessed the worm load after death at 6.5 months; the number of lambs studied was 501 between 1992 and 1995. We used standard parasitological methods to estimate egg counts and worm burdens1. Larval culture and post-mortem analyses indicated that more than 80% of the parasites present were Ostertagia circumcincta. At least 25 randomly chosen female O. circumcincta were measured for each sheep by image analysis (Foster-Findlay Associates Ltd).

The distributions of the numbers of O. circumcinctaadults and larvae were positively skewed and we transformed the data by taking the logarithm of each trait plus one. We estimated host heritabilities and genetic correlations by residual maximum likelihood fitting an animal model with all known pedigree relationships2. We calculated standard errors from the second derivative of the log likelihood profile around the parameter estimate.

The host heritability estimates were 0 for the number of fourth-stage larvae, 0.08 ± 0.09 for the number of fifth-stage larvae (sexually immature adults) and 0.14 ± 0.10 for the number of adult worms. There is no evidence in these results that genetic variation in the natural host influences the worm burden. In contrast, the heritability of worm length was remarkably high at 0.62 ± 0.20. This high heritability indicates that genetic variation in the host accounted for almost twice as much of the variation in mean worm length as all other factors combined. There was a strong phenotypic correlation between the number of eggs in the worm uterus and worm length (r=0.7; P in utero was also very high at 0.55 ± 0.19. An increase in mean worm length is associated with an increase in worm fecundity (Fig. 1). The heritability of faecal egg count at 6 months of age was 0.33 ± 0.14.

Figure 1: Relationship between worm fecundity and mean worm length.
figure 1

Fecundity was estimated from the log-transformed faecal egg count at slaughter divided by the log-transformed adult worm burden. The 95% confidence limits are shown.

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Our results indicate that in a flock of grazing lambs, the genetically resistant hosts3 reduce nematode egg production by decreasing worm fecundity. Although variation in egg output will be influenced by variation in worm burden and worm fecundity, there is no indication that variation in worm burden is under genetic control, at least in lambs.

We find little genetic variation in the number of fourth-stage larvae and suggest that arresting larval development is not an important mechanism of resistance to natural infection in lambs. Previous trials4,5,6with deliberate infections have indicated that the main immunological mechanism that regulates worm length and fecundity of O. circumcincta is the quantity and specificity of parasite-specific immunoglobulin A (IgA). The quantity and specificity of IgA may therefore be an important means of identifying resistant and susceptible lambs.