Can disease resistance evolve independently at different ages? Genetic variation in age-dependent resistance to disease in three wild plant species

1. Juveniles are typically less resistant (more susceptible) to infectious
disease than adults, and this difference in susceptibility can help fuel
the spread of pathogens in age-structured populations. However
evolutionary explanations for this variation in resistance across age
remain to be tested. 2. One hypothesis is that natural selection has
optimized resistance to peak at ages where disease exposure is greatest. A
central assumption of this hypothesis is that hosts have the capacity to
evolve resistance independently at different ages. This would mean that
hosts populations have a) standing genetic variation in resistance at both
juvenile and adult stages, and b) that this variation is not strongly
correlated between age-classes so that selection acting at one age does
not produce a correlated response at the other age 3. Here we evaluated
the capacity of three wild plant species (Silene latifolia, S. vulgaris,
and Dianthus pavonius) to evolve resistance to their anther-smut pathogens
(Microbotryum fungi), independently at different ages. The pathogen is
pollinator-transmitted, and thus exposure risk is considered to be highest
at the adult flowering stage. 4. Within each species we grew families to
different ages, inoculated individuals with anther smut, and evaluated the
effects of age, family and their interaction on infection. 5. In two of
the plant species, S. latifolia and D. pavonius, resistance to smut at the
juvenile stage was not correlated with resistance to smut at the adult
stage. In all three species, we show there are significant age*family
interaction effects, indicating that age-specificity of resistance varies
among the plant families. 6. Synthesis: These results indicate that
different mechanisms likely underlie resistance at juvenile and adult
stages and support the hypothesis that resistance can evolve independently
in response to differing selection pressures as hosts age. Taken together
our results provide new insight into the structure of genetic variation in
age-dependent resistance in three well-studied wild host-pathogen systems.