Plant sex and its impact on the evolution and ecology of plant defense

Plants exhibit myriad chemical and physical defenses that inhibit attack by insects and pathogens, but vary in effectiveness among plant species. Several ecological and evolutionary hypotheses have been proposed to explain this variation in defense, and although these hypotheses adequately explain variation in some systems, they fall short of a general predictive framework for the evolution of defense traits across plant species, and their ecological consequences for herbivores. We propose that existing theory on the evolution of sex provides robust and general predictions for the evolution of defense. This project tests specific predictions about the effects of plant sexual reproduction on the molecular and phenotypic evolution of defense in plants against insect herbivores, and the ecological consequences of these defenses for plant-insect interactions.

Sexual reproduction confers an advantage over asexual reproduction via two non-exclusive mechanisms: reduced linkage among alleles affecting fitness, and coevolution. The theories underlying these mechanisms give rise to the hypothesis that a loss of sex in plants should lead to the concomitant accumulation of deleterious mutations and reduced ability of plants to evolve defenses against their natural enemies, tipping coevolution in favor of parasites like insect herbivores and plant pathogens. Based on this hypothesis, I predict that a reduction in recombination and cross-pollination in plants will lead to: 1) an accumulation of deleterious mutations in defense genes subject to purifying selection (i.e., selection that prevents functional changes to genes), 2) reduced rates of adaptive evolution for genes subject to positive selection (i.e., selection that causes functional changes to a gene), 3) reduced levels of plant defensive compounds effective at deterring attack by parasites, and 4) increased damage by herbivores and pathogens which leads to larger reductions in fitness due to herbivore and pathogen attack.

We are examining these predictions using the Evening Primrose family (Onagraceae), which contains many plant species that undergo sexual reproduction (cross-pollination and meiotic recombination), as well as over 50 plant species that employ a functionally asexual reproductive system called permanent translocation heterozygosity (PTH), in which there is a breakdown of meiotic recombination, balanced lethal mortality of gametes, and almost exclusive self-fertilization. In collaboration with colleagues at Duke University (Drs. Mark Rausher and Stacey Smith) and the University of British Columbia (Sally Otto and Rich Fitzjohn), we arepeforming an ancestral state reconstruction to determine the number of independent origins of the PTH system across the Onagraceae. We are using this information to conduct a phylogenetically controlled comparative study of sexual and PTH species that will allow us to test the ecological and evolutionary predictions described above.

To test predictions 1 & 2, we are examining how transitions from sexual to asexual reproduction in the Onagraceae alters molecular evolution in a biosynthetic pathway that plays a critical role in plant defense - the flavonoid pathway. The flavonoid pathway is ubiquitous in plants and in the Onagraceae it produces many compounds (e.g., quercitens, myrcetins, kaempferols, tannins) that negatively affect herbivores and pathogens. We have started to clone genes in this pathway so that we can compare the history of selection on these genes between sexual and PTH species. To investigate predictions 3 & 4, we have been conducting greenhouse and field experiments in which we are measuring plant resistance traits, herbivory, and plant fitness in the presence and absence of herbivores.