The Effect of Evolutionary History on Plant-Insect and Plant-Pathogen Interactions

Abstract

It is impossible to overstate the importance of plants to life on this planet, and in terms of global carbon flux and food chains, autotrophic plants are among the most important organisms on Earth. The rise of photosynthetic plant life as a dominant force on earth altered the atmosphere into the oxygen rich air we breathe and sustains the food web we require to survive. This rise in available oxygen happened slowly at first, with cyanobacteria gradually releasing their waste as oxygen into the early oceans, and suddenly rose with a dramatic increase in atmospheric oxygen during the Great Oxidation Event. While this event was a death sentence for the large population of anaerobic organisms living at the time, it has allowed the enormous families of oxygen-dependent forms of life that we know today. Among all multicellular organisms, only plants have the ability to convert sunlight into organic substances via photosynthesis and are therefore able to live a more or less independent life, and their presence has shaped the ecosystems around them ever since. Humans have depended on plants since prehistory to satisfy their basic needs such as food, clothing, shelter, and medicine. One of the most serious and urgent threats to both agricultural and ecological plant systems are invasive species, especially invasive insect herbivores and plant pathogens that pose threats to plant health globally, resulting in significant ecological and economic damage.Prior to the age of human exploration, dispersal of species from one area to another was constrained by geographical, climatological, and biological barriers. For example, species were generally unable to cross oceans or mountains, could not survive a journey across a desert, or simply lacked the ability to move long distances. Consequently, the movement of species into new areas was limited to rare, stochastic dispersal events (i.e., such as those that were atmospherically-mediated), or relatively slow events such as continental drift or temporary land bridges due to global climate changes. While the ebb and flow of species is a natural process, the anthropogenic movement of species has accelerated their introduction into novel habitats. It is widely recognized that most non-native insect, pathogen, and weed species arrive in their new locations as a result of global trade and travel, and species may be transported inadvertently with their hosts when nursery stock, produce, or related commodities are shipped. Humans have transported and traded plant and animal species for millennia, with notable jumps in volume following European global expansion beginning in the 1500s, the industrial revolution, and in recent decades during the age of modern transportation mechanisms. With current trends in global trade, invasive species have caused, and will continue to cause, enormous ecological and economic damage, and understanding and managing invasive species are critical for protecting and restoring resilient ecosystems. Invasive species of all types can pose considerable harm to ecosystems, ecological processes, and both local and national economies, and can substantially alter the composition, structure, or function of native terrestrial and aquatic systems. Fortunately, only a minority of the species that arrive in a new environment are thought to successfully establish, and only a minority of them rise to the level of a high impact invasive species. Indeed, studies have found that about 10 percent of invasive species survive transport and introduction, about 10 percent of those that survive are able to establish to self-sustaining levels, and only about 10 percent of those cause significant ecological or economic damage (Williamson & Fitter 1996). This small minority of invaders, however, cause high impacts exceeding US$70 billion annually just in North America, which makes it imperative to predict which species pose the greatest risk The ability to implement eradication strategies against invasive species tends to be feasible only over a relatively short window. Before and just after a successful introduction, prevention and eradication are relatively low cost and have a higher probability of success. However, as invasive species become established over a larger area, the cost rapidly increases and the effectiveness of remedial measures rapidly decreases, making control economically infeasible or realistically impossible. It is therefore critical to identify and implement control measures early. Regulatory measures focused on prevention and early detection of alien pests include the listing of quarantine pests and plant passports/quarantine inspections, but such interventions can be hampered by a lack of knowledge on potential pests and novel pest-host interactions. Moreover, because many invasive insects and pathogens pose little harm in their native habitat, and thus are often unknown to managers, there tends to be critical knowledge gaps when they are introduced into a novel environment. Plants are also not passive organisms that merely sequester CO2 from the atmosphere until they are eaten, and nature is full of examples of plants influencing their environment, herbivores, pollinators, and other co-habitants. Co-evolution between herbivores and their plant hosts, as well as pressures from competition, predation, and parasitism, contribute to the complexity and stability of natural ecosystems. Two hypotheses in invasion biology consider the role of coevolutionary relationships in non-native species establishment and impact. One, the enemy release hypothesis, states that introduced species establish and spread because they are liberated from their co-evolved natural enemies. This hypothesis is supported with empirical support in the success of classical biological control strategies. The second, the defense free space hypothesis, states that a lack of adequate defenses in evolutionarily naïve hosts creates opportunities for non-native species to establish due to their lack of coevolutionary history with the invader. Lack of coevolved defenses against some invasive herbivorous insects has been documented, but relatively few studies have focused on this relationship. Only recently have quantitative studies looked at if and how these evolutionary relationships affect species invasiveness, with evidence suggesting that the divergence time between native and novel plant hosts is predictive of herbivorous insect impact. Studies that attempt to address the potential role of evolutionary history on interactions between plants and non-native herbivores and plant pathogens could benefit from the use of the plant collections within botanical gardens. Indeed, botanical gardens are recognized for their value in biosecurity research, such as the use of sentinel host plants to identify insect and pathogen incursions. Botanical gardens contain a diverse collection of native and non-native plant species, and are often located in urban areas, which places them in close proximity to high-risk introduction sites including sea ports, airports, and human dwellings. Arboreta and botanic gardens amass collections of plants from all over the world and, unintentionally, insects and plant diseases from other regions, which presents the serendipitous opportunity to identify and document new associations between plants and the pests and diseases that attack them. Botanic gardens have an institutional capacity to contribute to scientific studies of these pests and diseases, stemming from the living and preserved collections of plant diversity they develop and curate, coupled with their expertise in plant taxonomy, identification, propagation, and cultivation. Due to the plant resources available at the University of Washington Botanic Gardens, I used some of its plant collection for field experiments in support of my PhD dissertation research. During the time I conducted my field research, the Washington Park Arboretum was managed cooperatively by Seattle Parks and Recreation and the University of Washington. Within the physical space of the Washington Park Arboretum, the plant collections are a critical element of the educational, research, and outreach mission of the University of Washington. The property that constitutes the present Washington Park Arboretum includes two north-south ridges and the valley between, and is characterized by the natural drainage of small streams running north into wetlands and to Union Bay. The plant collections include over 14,500 accessioned specimens in the collections; over 4,000 different types of trees, shrubs and other plants native to 98 countries, which serve as vital resources for scientific study. For my doctoral research, I conducted three studies, each approaching the protection of plant collections from invasive species from a different perspective. In the first chapter, I conducted a field and laboratory-based study to measure the relationship between an introduced insect herbivore, the mountain ash sawfly (Pristiphora geniculata (Hartig)) and host species within Sorbus from around the world. In this chapter, I tested the hypothesis that host species from the native range of P. geniculata, presumed to be Europe, would have more effective co-evolved defenses against this folivore, resulting in reduced larval feeding performance and fitness as proxied by pupal weight, relative to evolutionarily-naive host species, such as those native to Asia and North America. In the second chapter, I used data collected on an introduced insect herbivore, the cherry bark tortrix (Enarmonia formosana (Scopoli) (Lepidoptera: Tortricidae), and a fungal pathogen that causes cherry brown rot (Monilinia fructicola Wint. and Monilinia laxa Aderhold & Ruhland) over a 10-year period. This dataset was used to evaluate the response of Prunus spp. from different subgenera and different native regions, as well as various climactic conditions, to cherry bark tortrix and Monilinia spp. In the third chapter, I conducted a literature review to predict, using published models, which insect species native to Asia but not yet established in North America are most likely to threaten woody plants native to the Pacific Northwest. Each of these studies will advance our understanding of the role of evolutionary history on plant-insect and plant-pathogen interactions.