Natural Selection on Individual Variation in Tolerance of Gastrointestinal Nematode Infection

Abstract

A 25-year study of wild sheep shows that individuals vary in how quickly they lose weight as parasite infections increase, and that those who lose the least weight when heavily infected produce more offspring.

Abstract

Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host–parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.

Author Summary

Animals can defend themselves against parasites through either resistance (reducing parasite numbers, for example, by killing them) or tolerance (maintaining health as infections levels increase, for example, by repairing damage). Resistance has been well-studied in wild animals, but tolerance has been less so. We analysed data on body weight collected over 25 years on a natural population of Soay sheep, infected with parasitic gut worms. As parasite burden increased, sheep lost weight. Crucially, there was variation among individuals: some lost weight rapidly with increasing infections (i.e., showed “low tolerance”), whereas others lost weight slowly (i.e., showed “high tolerance”). The least tolerant individuals lost 4.5 kg of body weight across the range of parasite burdens that we saw, whereas the most tolerant lost only around 0.36 kg. However, variation in tolerance did not have a heritable genetic basis, so that although tolerance varied between individuals, this was not due to genetic differences. Further analysis revealed that there was natural selection on tolerance. Individuals who were more tolerant of infection produced more offspring over the course of their lives. This study shows that natural selection can act upon resistance and tolerance simultaneously in nature, a result that has implications for both human health and livestock management.