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The cost of host genetic resistance to parasites in the domestic sheep: insights from a selection experiment
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Edité par CCSD -
International audience. Gastrointestinal nematode parasites are a growing concern for the development of grazing livestock systems as they cause major production losses and are increasingly resistant to different classes of anthelminthic drugs. It is now clear that solely relying on drugs to control parasites on farms is unsustainable. In contrast, sustainable strategies likely integrate different practices, among which the genetic selection of resistant animals can be key. Such selection is feasible but its side effects on production traits remain unclear. For instance in sheep populations, genetic correlations between host resistance and growth or reproductive traits are usually close to zero. This suggests that genetic trade-offs between host resistance and fitness-related traits do not occur in general despite the assumption that physiological costs of host resistance exist. Yet, genetic correlations from populations exposed to heterogeneous conditions may poorly reflect the consequences of physiological constraints acting at the within-individual scale. Selection experiments under controlled conditions can shed light on the mechanistic basis of evolutionary trade-offs. This research avenue has been seldom considered in livestock species although multiple selected lines on host resistance have been developed across various countries. Here, we present the main insights of a selection experiment in domestic sheep that we specifically developed to tackle the question of potential trade-offs. For over four generations we have divergently selected sheep indoor on their resistance to an artificial infectious challenge with Haemonchus contortus. Using several infectious challenges on those selected lines, we investigated three main aspects relative to the costs of host genetic resistance. First, we assessed the effects of selection for resistance in lambs on production traits at various life stages, in particular during the periparturient period of ewes when resource allocation to immunity may limit host resistance. Second, assuming that selection for host resistance could favor a preferential resource allocation to immunity at the expense of biosynthesis, we analyzed the feed efficiency (i.e. the conversion of feed intake into biomass produced) of our selected lines. Finally, we inferred the magnitude of the energetic cost of host resistance by fitting a mathematical model of host-parasite interaction to our experimental data. At first sight, our results provided little evidence for genetic trade-offs between host resistance and production traits or feed efficiency, in line with the genetic correlations usually found in other sheep populations. However, we observed that the expression of host resistance was strongly limited during the periparturient period, even when sheep were fed a nutrient-rich diet. Further, we detected small costs of resistance on body weight among ewes around their first lambing. Finally, we found that in infected lambs there was a low fat gain in the resistant line compared to the susceptible line that was consistent with a transient energetic cost of host resistance in our mathematical model. Specifically we estimated that resistant sheep allocated up to 15% of their energy intake to resistance to parasites, that is about three times more than susceptible lambs on average. Overall, we thus suggest that the lack of significant relationship between host resistance and other traits usually observed at a population level does not imply the absence of energy cost of host resistance at the individual level, although those latter costs can be particularly challenging to detect. Nonetheless, further research is needed to explore how those costs of host resistance affect population responses to selection under field conditions (e.g. repeated infection, period of underfeeding). Deciphering those mechanisms will help to develop parasite control strategies on farm that optimally combine the genetic selection of host resistance with other practices (e.g. nutrition, targeted treatments). It also provides an opportunity to promote exchanges between livestock and ecological sciences to increase our mechanistic understanding of life-history trade-offs in the context of host-parasite interactions.
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