Plant-herbivore interactions play an important role in the ecology and evolution of terrestrial ecosystems, yet the factors contributing to variation in the levels of plant defense remain poorly understood. We used a comparative phylogenetic approach to examine a previously untested hypothesis (Recombination-Mating System Hypothesis) which posits that the degree of meiotic recombination and segregation limits the rate at which plant populations adapt to herbivores and purge deleterious mutations.  To test this hypothesis we studied plants in the Onagraceae, which contains multiple species with functional recombination and outcrossing, as well as many species that are functionally asexual. We inferred the phylogeny of this group and performed ancestral state reconstructions of sexual versus asexual reproduction. Based on these analyses we selected multiple species that represented independent transitions between sexual and asexual reproduction for experiments to assess variation in resistance.
Results/Conclusions

We estimated that 21 independent transitions occurred between sexual and asexual reproduction.  Based on these analyses we selected 25 species from eleven independent transitions between sexual and asexual reproduction. We grew replicate plants from each species in a common environment and assayed resistance to two generalist herbivores (a caterpillar, Spodoptera exigua; and a mite, Tetranychus urticae) and one specialist herbivore species (Altica foenae) using feeding trial assays.  After accounting for phylogeny, caterpillars consumed 78% more leaf tissue (P = 0.01) and gained 64% (P = 0.003) greater mass on asexual than sexual plant species.  Survival of mites was 16% higher (P = 0.006) on asexual than on sexual taxa.  Resistance to S. exigua and T. urticae was correlated across plant species (r = 0.50, P = 0.009) suggesting that common mechanisms of resistance influenced both species. Trait-based data suggested that structural and physiological leaf traits (leaf toughness and specific leaf area), but not secondary chemistry, consistently differ between sexual and asexual species and may causally influence resistance to herbivores. In contrast to the effects on generalist herbivores, leaf consumption by the specialist A. foenae did not differ between sexual and asexual species and resistance to this herbivore was uncorrelated with resistance to generalist herbivores. To understand whether these same patterns occur in the field, we conducted a field experiment. Several generalist herbivore species fed on plants and they imposed 75% greater herbivory (P = 0.02) on asexual species than on sexual species.  Our results suggest that variation in meiotic recombination and segregation may play an important yet overlooked role in shaping plant defense.