Plants have evolved an array of traits that protect them against damaging insects, and different plant species vary dramatically in their level of chemical defenses. Despite substantial progress in understanding the biology of plant chemistry, a basic understanding of the evolutionary mechanisms that cause plants to vary in defense is lacking. Recent results suggest that differences in the reproductive strategies used by plants might play an important role. Specifically, reproductive systems that result in the loss of genetic diversity may also result in lowered defense. The goal of this project is to better understand whether different plant reproductive strategies influence the ability of plants to maintain defenses against insects, and to elucidate the genes that cause such evolutionary change.
Interactions between plants and insects are of critical importance to natural and managed ecosystems as insects consume a large proportion of the biomass produced annually by plants. Such damage costs billions of dollars in lost revenue to farmers and foresters each year. It is therefore important to understand how plant species defend themselves and why they frequently vary in the types and levels of defenses they employ against insects. This project will help to elucidate the evolutionary and genetic causes of variation in plant defense observed among plant species, and ultimately provide a better understanding of the biological interactions within natural and managed ecosystems.
Plants form the base of virtually all food webs on earth and are the foundation on which much of human society is built. Plants provide us with food, shelter, medicine, aesthetics, inspiration for art and design, and a wide variety of ecosystem services. At the same time, plants are under constant threat from a wide diversity of organisms seeking to eat, infect and parasitize every part of a plant. Providing secure and stable production of plants for human and ecosystem services requires a comprehensive understanding of how plants defend themselves against the numerous insects and pathogens seeking to consume and parasitize them. When we look out into nature we see that some plant species are constantly devoured by insect herbivores while others are left untouched. Many of the "protected plants" are chalked full of toxic chemicals or protected by armor like thorns or stinging hairs, while others seem rather defenseless against a battery of would-be attackers. Why do we see this variation and how might it evolve in nature? In this project we sought to test a new hypothesis - plant sexual reproduction plays a critical role in affecting the ability of plants to evolve novel defenses and to maintain the functionality of existing defenses. Using the evening primrose plant family as a model (Onagraceae), where there have been numerous transitions between sexual reproduction and functionally asexual/clonal reproduction, we examined the ecology, chemistry, physiology and the evolution of plant genes and proteins underlying plant defenses against insect herbivores and plant pathogens for numerous plant species. We found that asexual plants tended to live at higher latitudes than closely related sexual plant species, and they evolved decreased investment in costly floral structures (e.g. flowers, floral tubes, pollen) used primarily for sexual cross-fertilization. We also discovered that plant defenses were impaired in asexual plant species, where the production of chemical and physical defenses were lower in asexual compared to sexual plant species. These decreased defenses were correlated with increased damage by generalist feeding insect herbivores. The loss of sex also affected the molecular evolution of plant defense genes involved in resistance to fungal pathogens, as we found that sexual plant species were more likely to evolve novel beneficial genetic mutations fixed by natural selection, and they were also more likely to maintain high levels of expression in genes critical for defense than their asexual counterparts. Finally, and somewhat surprisingly, despite the apparent advantages of sexual reproduction in defenses against parasites, asexual reproduction is common among the evening primroses and does not appear to represent an evolutionary dead-end, as has long been predicted by biologists. Instead, asexual plant species tend to give rise to new species more readily via a process called "speciation" than sexual plant species, and we could not detect any difference in rates of extinction, resulting in net diversification rates being higher in asexual lineages. Furthermore, asexual lineages were able to regain sex over time once it had been lost, which had previously thought to be a rare if not impossible process. Overall the results from this project suggest that plant sexual reproduction plays a critical role in the ecology, evolution and diversification of plants, especially as it relates to their defenses against plant parasites.
