Parasite defense covaries with reproductive timing, not with resistance

Abstract

Defense is the ability of a host to minimize fitness loss to parasites. It is among the most variable phenotypes in host populations, and this variation facilitates rapid adaptation under parasite-mediated selection. We do not, however, know the underlying host traits that explain this variation in defense against parasites. A common assumption is that the most defended hosts are the most resistant, meaning they limit the establishment and growth of infecting parasites. Under this assumption, resistance traits should evolve readily under parasite selection. Resistance is, however, just one of many strategies hosts use to defend against parasites, and it does not consistently covary with fitness in the presence of parasites. We accordingly asked: which host traits covary with defense against parasites? We use controlled exposures to characterize genetic variation in defense of the nematode Caenorhabditis elegans against its natural microsporidian parasites. We report extensive variation in defense among wild strains of C. elegans: some strains lost 60% of fecundity under parasite exposure, while others were unaffected. We then tested the covariance of defense with two prominent host traits, resistance and reproductive timing. Our results did not support the hypothesis that resistance covaries with defense: strains with lower parasite burden did not have higher relative fecundity under exposure. Our results instead supported the hypothesis that life history covaries with defense: host strains that reproduced quickly had higher relative fecundity under exposure, consistent with the idea that parasites diminish future reproductive opportunities. The observed variation in defense among host strains indicates significant potential for wild C. elegans populations to evolve in response to their natural parasites. Because reproductive timing underpins this variation in defense, parasite-mediated selection could operate directly on host life history traits and should also be highly sensitive to shifts in life history driven by other biotic and abiotic factors. AUTHOR SUMMARYSome hosts fare much better than others in the face of parasite infection. What traits differentiate defended hosts from undefended hosts? The answer to this question is critical for identifying the strategies that best protect hosts from their parasites. It also allows us to predict and interpret the evolution of host populations over the course of epidemics. To address this question, we surveyed wild strains of a tractable model host, the nematode Caenorhabditis elegans, for their response to two species of microsporidian parasites. We found that, on average, parasite exposure substantially impaired the ability of hosts to reproduce. Host strains, however, varied widely: some experienced major losses in fecundity with exposure, while others were highly defended, showing little to no change. We identified reproductive timing as a key trait that differentiated defended hosts from undefended hosts. Our results suggest that reproducing quickly may have been protective, by allowing hosts to make most of their offspring before parasites impaired reproduction. We did not find evidence that resistance was protective: host strains with lower parasite burdens did not reproduce better than those with high parasite burdens. These findings give added weight to life history as a major component of host defense against parasites.