Jeffrey L. Feder - US grants

9508559 FEDER The Tephritid fly Rhagoletis pomonella is of interest to both farmers and population biologists alike. Not only are these flies major economic pests of apples, but they may also be in the process of speciating. Although R. pomonella is commonly referred to as the "Apple Maggot", apples are not the native host plant of these flies. That distinction belongs to hawthorns (thornapples). In the mid-1800's a portion of the R. pomonella populations in the Hudson Valley region of New York shifted from hawthorns and started attacking apples as a new host plant. Since then, apple-infesting populations of R. pomonella have spread across the eastern United States and have recently been introduced into California, Oregon and Washington. Genetic studies indicate that apple and hawthorn populations of R. pomonella are partially isolated entities. Six genes consistently display frequency differences between the apple and hawthorn fly races. These studies suggest that Rhagoletis flies may speciate sympatrically (i.e. without geographic isolation) in the process of specializing on new host plants. The goals of the proposed research are two-fold:1.) To ascertain how R. pomonella has adapted its life history to allow it to successfully attack apples as a new host plant. 2.) To determine the role that such changes in life history play in isolating apples from hawthorn races of the fly. Because R. pomonella flies have only one generation per year and adults live for only about a month, there is strong selection pressure on apple and hawthorn flies to match their development to that of their respective host plants. To test this hypothesis, Dr. Feder will manipulate rearing conditions for flies in the laboratory to induce environment dependent changes at the six genetic markers differing between the host races. In effect, he will be attempting to genetically transform the hawthorn host race into the apple race (and vice-versa) by selecting on hawthorn flies as if they were infesting f ruits with the earlier phenology of apples. What will we learn from the proposed research? First, the experiments will elucidate whether and how R. pomonella has altered its life history so that it can attack apples. Second, the results will pinpoint which environmental factors are most important for R. pomonella to overcome in a successful host shift. By subsequently measuring the intensity with which these factors act in the field, it will be possible to gauge how effective host-associated selection is at reproductively isolating apple and of the development traits adapting R. pomonella to apples. Such information will aid us in devising new measures to control the Apple Maggot and other fruit fly pests. The results will also help us predict what crops are potentially vulnerable to attack by Rhagoletis, as this pest spreads into new, fruit growing regions of the United States. Dr. Feder also has a strong commitment to transfer knowledge of population biology to others. This CAREER grant will also allow him to continue to pursue his teaching interest. He will teach a series of three classes at the undergraduate and graduate levels, exposing students to the general principles and concepts that form the basis for this and other research in population biology & systematics.

One of the most pervasive questions in evolutionary biology is; how does speciation takes place. To address this question, Drs. Feder, Roelofs and Berlocher will be examining the genetic architecture for both the behavioral components and the life history responses to seasonality in a complex of very similar host races in the genus Rhagoletis, tephritid fruit flies. Species in this genus have long been an excellent model for the study of speciation and this work builds on this solid basis. In a well-orchestrated project, these investigators will bring the tools of molecular genetics and chemical ecology to bear on this problem. Using two interfertile host races which vary in the traits of interest, the locations for genes responsible for behavioral components of host plant selection, including the responses to plant produced volatile chemicals, will be mapped. Genes for determining when the inactive, over wintering phase of the life cycle ends will be mapped as well. These traits are known to be of important in maintaining the separateness of the host races in nature.

Results of this work will provide important insights regarding the mechanism of speciation. In addition, the project will support research experiences for undergraduate and graduate students. Finally, tephritid fruit flies are important agricultural pests so that the basic understanding regarding speciation in this group, while of general scientific interest, may also have relevance for pest control.

This Integrative Graduate Education and Research Training (IGERT) award supports the establishment of a new interdisciplinary graduate program in Global Linkages of Biology, Environment and Society (GLOBES) at the University of Notre Dame. The program integrates research, training, and educational activities among complementary faculty in ecology, evolution and environment, infectious disease, and social science, ethics, law and economics. The goal of the program is to train a new generation of Ph.D. scientists capable of designing and implementing sound scientific solutions to environmental problems within the framework of human culture, economics, policy, and law. Human practices and activities affecting environmental and global health have interrelated causes and feedbacks. These feedbacks are both biological and social, and exacerbate environmental degradation and the spread of invasive species and disease. Consequently, solutions to increasingly linked environmental and health problems require the coordinated interaction of biological and social scientists with expertise in ecology, evolution, infectious disease, anthropology, ethics, law, policy, and economics. The intellectual merit of this IGERT consists of the integration of the research and education activities of life and social scientists at the University of Notre Dame in a concerted effort to understand and find solutions to five specific problems: (1) invasive species in the Great Lake and their cascading effects on ecosystems (2) interactions of human land-use change and malaria transmission in West Africa; (3) cross-primate exchange of disease on the island of Bali, (4) resurgence of schistosomiasis in China driven by changes in water- and land-use patterns, and (5) impacts of invasive Sudden Oak Death as it spreads across the U.S. Without interdisciplinary thinking, relatively simple and effective measures to reduce environmental damage and disease transmission can go unrecognized. Most analyses suffer from concentrating on only one aspect of the question (e.g., ecology, culture, or disease). This IGERT will foster cross-disciplinary conversation and guide research directed at developing prevention and control responses to invasive species and disease that are scientifically sound, culturally acceptable, and cost-effective. The IGERT will use a coordinated set of approaches ranging from team-based research projects to outreach service activities to provide students with the interdisciplinary skills and knowledge they need to tackle the increasingly complex environmental and global health problems of our nation and the planet. The broader impacts of this proposal include finding solutions to these environmental and health problems. IGERT is an NSF-wide program intended to meet the challenges of educating U.S. Ph.D. scientists and engineers with the interdisciplinary background, deep knowledge in a chosen discipline, and the technical, professional, and personal skills needed for the career demands of the future. The program is intended to catalyze a cultural change in graduate education by establishing innovative new models for graduate education and training in a fertile environment for collaborative research that transcends traditional disciplinary boundaries.

The intellectual and scientific focus of the research centers on how new species of Rhagoletis pomonella fruit flies form. Speciation occurs as genetic barriers to gene flow evolve between populations that cause them to become reproductively isolated from one another. Traditionally, speciation has been thought to require that populations be completely geographically isolated by physical barriers to movement (e.g., mountain ranges, large rivers, oceans). By precluding individuals from moving between populations, geographic isolation results in genetic changes occurring independently between populations which, over time, can accumulate to the point that the populations evolve into reproductively isolated species. The apple maggot fly, Rhagoletis pomonella, has been argued to be a possible exception, however. As early as 1864, Benjamin Walsh hypothesized that certain insects that specialize on attacking specific plants could speciate without geographic isolation ("in sympatry") in the process of them shifting and ecologically adapting to new host plants. In particular, Walsh cited the shift of Rhagoletis pomonella from its native host plant hawthorn (Crataegus) to introduced, domesticated apple trees in the United States - an event that occurred in the 1850's - as a real time example of his idea of sympatric speciation in action. Subsequent genetic studies have confirmed Walsh's hypothesis that the apple and hawthorn-infesting forms of Rhagoletis pomonella are partially reproductively isolated "host races", potentially in the first stages of diverging into new species. An important factor responsible for the divergence of the apple and hawthorn flies is that apple and hawthorn trees fruit at different times of the year, resulting in the one-generation per year life cycles of apple and hawthorn flies having to be offset in order for them to be able to attack apple vs. hawthorn trees. Recently, an interesting twist to the Rhagoletis story has been discovered. Some of the genes responsible for the difference in the life history of apple and hawthorn flies in the United States may have originated over a million years ago in an isolated population of hawthorn-infesting flies in Mexico. These genes were introduced into the U.S. in the distant past during a period when the Mexican and US hawthorn-fly populations came into contact (perhaps 500,000 years ago), and very recently these genes helped facilitate the shift to domesticated apple following the planting of apples in the US by European colonists. Thus, geographic isolation and gene flow may act in conjunction with ecological specialization to help trigger "sympatric" speciation events (i.e., the introduction of apples into the U.S. provided hawthorn flies with a new ecological niche - a temporal resource island - that they were able to take advantage of, in part, because of the genetic variation they possessed due to past gene flow from Mexico). The current grant proposal will test this biogeographic hypothesis thorough an extensive analysis of DNA sequences of genes located throughout the genome of Rhagoletis flies. The research will involve a survey of flies collected throughout Mexico to determine the extent of the geographic range of Rhagoletis flies in the country and pinpoint possible sources of gene flow into the U.S. in the past. In addition, the genetic analysis will indicated whether certain genes and genomic regions have characteristics that made them more or less prone to have moved into the US fly population (e.g., whether or not the genes reside within inversions - stretches of chromosomes that have different linear orders of genes along them - that have been hypothesized to retard gene flow between species). In this manner, the research will resolve the genetic history underlying the recent shift and formation of the new form of apple-infesting Rhagoletis pomonella.

The broader impacts and societal benefits of the research are multifaceted. The project will integrate science training and educational activities at the local, community, University, and international levels. The study will involve the participation of a Post-Doctoral associate and graduate, undergraduate, and high school students in various aspects of the work ranging from field and laboratory research to class modules designed to give high school students and educators hands on experience with molecular genetic techniques and analysis. The funding provided by the current proposal will also expand and strengthen the Population Biology program at the University of Notre Dame at a critical stage of its development. In addition, the proposed research represents an international collaboration between researchers at Notre Dame and two distinguished Mexican colleagues, Dr. Martin Aluja and Dr. Juan Rull, at the Ecological Institute in Xalapa, Veracruz. Drs. Aluja and Rull have received parallel support from CONACyT to fund the collaboration. Finally, the proposed Rhagoletis research has significant applied, as well as basic, scientific implications. Rhagoletis pomonella is a major economic pest of apples, and related species attack cherries, blueberries, and several other crops. The question of the extent and host range of Rhagoletis pomonella in Mexico has important implications concerning the import and export of fruit between the two countries, as well as how new populations of pest species form and can be controlled. The impact of the proposed research is therefore ranges from new basic and applied scientific findings, to educational and societal benefits.

The goal of this research project is to understand how the apple maggot fly, Rhagoletis pomonella, a major pest of apples, can form populations that specialize on different species of its native hawthorn food plants in the southern United States. Unlike insects such as grasshoppers, where all individuals of a given species can and do eat a wide range of food plants, the apple maggot and similar insects form local populations (termed "host races") that feed within the fruits of only one or a few plant species. To understand how they do this, fly populations attacking different species of hawthorns in the southern United States will be tested to determine: 1) if they preferentially orient toward the chemical odor of the fruit of the hawthorn species they infest--this is how the flies find their host plants in nature to mate on and lay eggs into fruit, 2) if the timing of the life cycle of the flies is adapted to differences in when the various hawthorn trees fruit--some southern hawthorns fruit very early in the season (May) and some late (October-November), and 3) the degree to which any observed differences in odor response and life cycle are genetically based.

The broader impacts of the research are multi-faceted, having both important applied and basic benefits. Insects frequently shift their feeding to new crops. The apple maggot fly is a classic example, having shifted in the last 100 years from native hawthorns of little commercial interest to introduced apples of great economic value. Information about how this process occurs, which will be provided by research on southern hawthorn flies, is needed for better management of pests. For example, Rhagoletis pomonella flies from apple are repelled by the odor of red hawthorn, and vice versa, leading to the possibility that even better natural repellent odors might be found among the various southern hawthorn species. The project is also of basic scientific interest because shifts onto novel plants may serve as a trigger for speciation for many host specific insects. Finally, the project will provide important additional societal benefits by helping integrate science training and education across the local, community, and university levels

Insect pests cause billions of dollars of damage to crop plants world-wide each year. With the continuing globalization of agriculture, crops are routinely introduced into new locations where they will come into contact with novel insect pests, and insect pests are frequently inadvertently introduced to new areas where they come into contact with novel crops. Therefore, a critical question is what are the factors that facilitate or prevent insects from becoming established on a novel plant? The apple maggot fly, Rhagoletis pomonella, is a model system for understanding how plant-feeding insects can move onto new hosts. These maggots are native to North America and historically fed on the fruits of hawthorn trees. However, after domesticated apples were introduced into the northeastern United States approximately 350 years ago by English and Dutch settlers, R. pomonella began feeding on apple fruits and has become a significant pest of domesticated apples. In areas where apples and hawthorns occur together, the two plants produce fruit at different times during the summer. The adult flies, which lay their eggs on the fruit, are short lived. This has lead to a separation in the timing of occurrence of the apple and hawthorn flies, which was critical for R. pomonella to become a pest of apples. Much is known about the genetics of life history timing and the shift onto apples in this fly, but little is known about the physiological traits that have facilitated the shift. This project will investigate the physiology of life history timing and determine if three critical physiological traits, fat storage, metabolic rate, and body size, differ between the apple and hawthorn flies, and determine if they are linked to specific genetic markers that are associated with differences in life history timing. This work will provide the first synthesis of physiology, genetics, and life history timing in a plant-feeding insect and will serve as a foundation for understanding how physiology may affect life history timing and either facilitate or prevent novel interactions between insects and plants, a critical question for both evolutionary biology and agriculture.

The PIs have a strong record in educational outreach and training, including traditionally underrepresented groups. This project will include training of postdocs, graduate and undergraduate students. Linking climate related physiology to insect host race formation will provide important information for understanding host range change and future pest problems as a consequence of climate variation.

This project will explore a "cascading" speciation event involving the apple maggot fly (Rhagoletis pomonella) and a parasitoid wasp (Diachasma alloeum) that hunts and consumes the fly's larvae. Populations of both of these organisms have made a shift from their ancestral host, the hawthorn tree, to introduced European apples. Past work has shown that this shift has resulted in the formation of apple- and hawthorn-associated "races" of R. pomonella, each adapted to their respective hosts. It is believed that these races are a first step towards formation of distinct species. This project will look for evidence of a parallel race formation in D. alloeum through differences in wasp life history, behavior and genetics.

The broader significance of this research is that it will help to form a more complete understanding of the processes underlying biodiversity. Phytophagous (plant-feeding) and parasitic insects are the most diverse organisms on Earth. One of the unifying goals in biology involves uncovering the sources of this spectacular diversity. Studying the evolutionary dynamics of such a tight ecological network of plants and insects should make clear some of the processes through which natural selection acts to create new species. Furthermore, this work will be of general interest to evolutionary biologists because it involves speciation in the absence of geographic isolation, an event for which few conclusive examples exist.

The project will determine whether the creation of new species provides an opportunity for other organisms to take advantage of this and speciate in kind. In particular, the research will test whether when fruit flies of the genus Rhagoletis speciate by shifting and attacking new host plants, the parasitic wasps that attack the flies also speciate by following the flies and specializing on the new fly resources. The question is important for understanding nature because there are more species of plant eating insects like Rhagoletis and the parasites that attack them than any other types of life forms on Earth. Thus, understanding whether speciation has rippling effects through ecosystems to sequentially amplify the creation of new species has important implications for understanding the basis for biodiversity.

In addition to helping integrate science training, education, and research activities at the local, university, and international levels, the project also has practical benefits for U.S. agriculture. Rhagoletis flies are serious pests of apples, cherries, blueberries, and several other economic crops. The question of whether the fly's parasitoids have formed new species, therefore, has important repercussions for developing effective integrated pest management strategies. Specifically, if different wasp species attack each fly, then biocontrol efforts would need to rear and release each of the wasps separately to control each of the fly pests. In contrast, if the wasps are all part of the same population, then a one-size-fits-all strategy focused on mass release of a single cultured wasp strain may succeed.

Organisms must time their lifecycles to avoid stressful periods of the year (e.g., winter cold and lack of resources) and to exploit the good times of the year when weather is favorable and resources are abundant. Dormancy responses have evolved in many organisms, from plants and microbes to mammals and insects, to achieve synchrony with local seasonal conditions. Organisms are increasingly challenged by new seasonal regimes caused by 1) contemporary climate change, 2) habitat modifications from human development and urbanization, and 3) movement of species into new areas through managed or accidental introductions. Thus, understanding how dormancy responses rapidly evolve and compensate for shifts in seasonality will be a critical component for understanding the persistence and spread of native and invasive species in our rapidly changing world. This research will characterize the mechanisms that allow rapid adaptation to novel seasonality via changes in dormancy in the apple maggot fly, Rhagoletis pomonella, a major pest of apples and a textbook example of rapid species formation. Within the last 200 years, R. pomonella has shifted from its native host hawthorn (Crataegus mollis) to introduced, domesticated apple (Malus domestica), and in the process has formed new, partially reproductively isolated populations on apples. Seasonal fruiting time differs substantially among plant species in a given region, so adapting to a novel fruit requires adaptation in insect seasonal timing. In R. pomonella, the newly derived apple population has become established on their novel host fruit via evolved differences in timing of the overwintering dormant stage, which results in temporal matching of insect growth and reproduction with earlier seasonal availability of apple compared to hawthorn fruits. Physiological mechanisms that evolve to adjust dormancy timing are poorly understood, and this research will leverage variation among the fly populations to quantify physiological differences in gene and protein expression and differences in the genome that underlie adaptation at key regulatory points across the fly life cycle. Additionally, experiments will address whether common physiological mechanisms underlie adaptation across the three phases of dormancy (dormancy induction, maintenance, and termination) potentially constraining the rate or direction of evolutionary responses to changing seasonality. This fundamental research has implications in numerous contexts from preserving biodiversity to forecasting agricultural production and the spread of invasive species. Beyond identifying important features facilitating rapid responses to seasonal change, the project will also enhance a pre-collegiate education program in evolutionary biology. Host race formation in R. pomonella provides a clear and intuitive example of ecological adaptation and the genesis of new crop pests, making the flies excellent ambassadors for evolution, a subject poorly understood by many students and the general public. The research team previously developed a workshop and outreach program for STEM education to enhance the evolution knowledge of high school teachers and students from Florida and Puerto Rico, providing materials for science curricula. The current grant will expand the high-school teacher training, add freely accessible web-based curricular materials, and most importantly, formally evaluate the impact of the educational program. Survey-based assessments delivered before, during and after the workshop will assess changes in perception of frequently misunderstood concepts in evolutionary biology.

Understanding the process by which new species evolve (speciation) is a fundamental question in biological sciences. A popular, but largely untested idea is that the formation of one species can catalyze the formation of other species within a community of interacting organisms (sequential speciation). Previous work has shown that a shift of the apple maggot fly from its native hawthorn host plant to the introduced domesticated apple about 150 years ago in the eastern US has induced a sequential host shift in the insect parasite community that attacks the flies. Specifically, as the fly shifts to attacking the fruits of a new host plant, the insect parasites that attack that fly shift in kind. What remains unknown is how general and rapid sequential speciation events are in nature. A powerful approach is to test the sequential speciation hypothesis in a more proximate case in the western US where the fly was recently introduced just 50 years ago. The proposed research will examine changes in the flies and their parasites in this new habitat to better evaluate the rate of speciation.

Understanding the origins of biodiversity is one of the central issues in biological sciences. In this regard, sequential speciation may be particular relevant for understanding biodiversity in general and in particular the astonishing levels of insect biodiversity (estimated 10-30 million species worldwide, the most diverse group of animals on the planet). Additionally, the apple maggot fly and several closely related species are major economic pests of several agricultural crops. Characterization of the origins of the parasitoid community can inform bio-control schemes to help farmers control the fly before it becomes a serious pest in the western United States.

The timing of seasonal life cycles is a critical question underlying many biological processes, including the generation and maintenance of biodiversity and agriculture production and food security. Animals and plants must synchronize their lives with the seasons to avoid freezing or overheating and to exploit seasonal resources. The goal of this grant is to understand how historic and contemporary shifts in seasonality can facilitate biological diversification in insect communities. In the short term, such shifts have caused rapid evolution of new crop pests and associated parasite communities. The proposed research tests 1) whether the same processes explain more ancient diversification of communities, and 2) whether changing climates will disrupt or promote diversification in the future. The results may inform many scientific fields, from basic research on the genesis of new species to applied control of agricultural pests. This project includes workshops with high school teachers and students to build curricula supporting "learning by doing" and meeting national standards, as well as providing training for graduate students and postdocs.

This project includes genomic analysis of dipteran pest insects, including the apple fly Rhagoletis pomonella and blueberry maggot fly Rhagoletis mendax plus the community of parasitoid wasps that attack these flies. Genomic work will integrate with 1) functional studies of the overwintering hibernation of both the flies and the wasps from hormonal and molecular perspectives, and 2) computational simulations of the responses of the flies and their parasites to projected seasonal shifts resulting from climate change.