Source: PENNSYLVANIA STATE UNIVERSITY submitted to
CHEMICAL ECOLOGY OF MULTI-TROPHIC INTERACTIONS AMONG INSECTS, PLANTS AND MICROORGANISMS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
1010058
Grant No.
(N/A)
Project No.
PEN04609
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Jul 1, 2016
Project End Date
Jun 30, 2021
Grant Year
(N/A)
Project Director
Baker, TH, C.
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
This project proposes to conduct research to find out how volatile chemical compounds affect insect behavior and physiology, and what these compounds are. The sources of these volatile chemicals come from damaged and undamaged plants, both the above-ground leafy and stem parts as well as the below-ground roots and stems. The sources also come from flowers and fruits, as well as from microorganisms living in the soil, on the roots, and on the leaves and above-ground plant structures. Very powerful volatile chemical sources are emitted by the insects themselves in the form of sex and aggregation pheromones that attract individuals from tens or even hundreds of meters away. Our project will use state-of-the-art techniques and instrumentation to to determine which volatiles or blends of volatiles from these various sources are responsible for altering insects' behaviors and physiologies. We will then devise ways to use these volatile chemicalsignal(semiochemical)blends to apply them in field situations to show their efficacy as tools for detecting, monitoring, and suppressing pest insect populations.
Animal Health Component
0%
Research Effort Categories
Basic
70%
Applied
20%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2113110200040%
2113110102020%
2063110100030%
2123130102010%
Knowledge Area
212 - Pathogens and Nematodes Affecting Plants; 206 - Basic Plant Biology; 211 - Insects, Mites, and Other Arthropods Affecting Plants;

Subject Of Investigation
3130 - Nematodes; 3110 - Insects;

Field Of Science
2000 - Chemistry; 1000 - Biochemistry and biophysics; 1020 - Physiology;
Goals / Objectives
1. Clarify and document the role of plant volatiles in chemical communication within and between plant species.2. Elucidate the role of plant volatiles in plant-pathogen-vector relationships and subsequent effects on disease transmission dynamics3. Document the effects of population genetic variation on plant volatile production.4. Identify the individual and combined effects of elicitors present in insect regurgitant on insect-induced plant volatiles.5. Develop technologies that employ plants in remote sensing of environmental information.6. Identify environmental conditions that affect plant biochemical changes elicited by insect herbivores on both direct and indirect plant defenses.7. Determine the existence of pheromone communication systems in target insect species and isolate and identify these pheromones for use in detection, monitoring, and mating disruption.8. Identify and evaluate chemicals that regulate or influence behaviors, including foraging, mating and oviposition, of important beneficial and pest insects.9. Determine physiological and biochemical mechanisms, elicitors, and regulators involved in the interactions of plants with insect herbivores, their natural enemies, and microorganisms.10. Determine the olfactory and gustatory neuronal pathways and the neuronal response profiles to odorants and tastants that underlie pheromone-mediated behaviors of insects.11. Understand cues in belowground contexts involving plant, herbivores and their natural enemies
Project Methods
1. Examination of within-plant volatile communication will be carried out through manipulative laboratory experiments in which we regulate air-flow between tree leaves known to share or not share direct vascular connections, as well as between individual plants of the same or different genotypes. For our work with trees, pairs of leaves with or without vascular and/or air connections can be subjected to various treatments and the responses of the treatment and target leaves can be assayed by measuring volatile production or assaying leaf chemistry. Volatile and leaf tissue collections and analyses will follow well established methods2. To date all previous research on herbivore saliva and Fatty acid-amino elicitors has been conduced separately; yet, we believe these two likely sources of plant elicitors occur together and interact to mediate herbivore-induced volatile responses.Using intact plant assays, we will first confirm that differences in induced volatiles exist following feeding by ablated and non- ablated Helicoverpa zea. Upon confirmation, we will focus on the interaction of crude saliva and on the volatiles induced by FAC elicitors. If significant interactions exist among FAC elicitors, saliva and volatiles, the specific action of GOX will be tested using purified GOX .3. In both cotton and tobacco, herbivory by the larvae of two closely related pest species, H. virescens and H. zea results in markedly different volatile profiles that differ in attractiveness to the parasitoid Cardiochiles nigriceps. Cardiochiles nigriceps is attracted to plant volatiles induced by its host and avoids volatiles induced by a non-host. Preliminary results suggest that factors (other than FACs) present in the saliva and regurgitant of herbivorous caterpillar species drive the differential emission of volatiles and ultimately parasitoid attraction. To test this, we will first closely compare the volatiles induced in tobacco by feeding damage of H. virescens, Spodoptera exigua and Manduca sexta larvae with ablated and non-ablated spinnerets.4. We will first closely compare the volatiles induced in tobacco by feeding damage of H. virescens, Spodoptera exigua and Manduca sexta larvae with ablated and non-ablated spinnerets. Potential differences in levels of feeding damage will be compensated by regulating the numbers of caterpillars used on each leaf. Investigation of systemically induced volatiles alone, with the insect feeding sites removed, can further isolate potential physical differences between plants. We will also conduct bioassays with plants damaged and treated with either saliva or regurgitant to determine the source of active compounds. Biologically active molecules that have different effects on plant defensive responses will be isolated and identified.5. To isolate and identify prospective insect sex pheromones, we will employ time-tested techniques for affirming both neurophysiological and behavioral activity, in addition to high-resolution gas chromatographic (GC) and mass spectrometric (MS) analyses. We will perform combined gas-chromatography/electroantennogram (GC/EAG) analyses on pheromone extracts and airborne collections from pheromone-emitting individuals. When necessary, electropalpograms (EPGs) will be used for GC/EPG analyses. When possible, we will also use a technique called coupled GC-Behavior Bioassay (GC/BB), which has been successfully used in the Baker lab recently. Extracts or airborne collections will be analyzed concurrently using high resolution GC/MS in our laboratories.6.Elicitors produced by insect herbivores that trigger plant biochemical defenses will be isolated, identified, synthesized and tested for biological activity. Key phytohormone signals and signaling pathways within plants that are modulated by insect produced elicitors, as well as antagonistic and synergistic interactions between signaling pathways, that alter plant responses to insect herbivore damage will be investigated. Additionally, we will study the effect of other factors like nutrition, water stress, and presence of plant pathogens and other microorganisms on the ability of plants to defend against insect herbivores.7.Belowground tritrophic interactions studies.This study's goals are to provide growers with new tools for: a) improved monitoring adult root feeding herbivores, and b) increased efficacy of entomopathogenic nematodes.Using custom belowground olfactometers and volatiles collection systems. We will analyze volatiles emitted from various plants while being feed upon by root pest insects. We will isolate and test the cues on beneficial nematode in behavioral assays, and identify which cues are attractive to these natural enemies. We will also evaluate and compare roots of plants for attraction and repulsion of root herbivores in behavioral assays. These isolated compounds will be tested for efficacy in laboratory and field experiments.8.Arbuscular mycorrhizal fungi (AMF) are known to affect nutrient uptake, chemical defense production, and production of volatile organic compounds (VOCs) in agricultural plants. Wewill address the following objectives: Obj 1 Determine the interactive effects of nitrogen, phosphorus, and AMF colonization on VOC and plant defense production in field corn; Obj 2 Determine cover crop effects on VOC and plant defense production in field corn, and whether the induced changes are due to cover crops' ability to alter soil N, P, and AMF colonization; Obj 3 Assess the ability of field corn to tolerate herbivory by three pest types - a foliar feeder, a stem feeder, and a root feeder - when grown in soil primed by different cover crop treatments; Obj 4 Assess whether corn VOCs, and oviposition response of three pest types to these VOCs, are altered by rearing plants in soil primed by different cover crop treatments.9. The understanding of olfactory sensory neuron reporting of the abundance and ratios of sex pheromone components and volatile components of kairomone blends has increased substantially during the last 20 years. Classes of odorant receptor proteins involved in the transduction of volatile molecules into neuronal action potentials are now known to include odorant receptors (ORs), ionotropic receptors (IRs) and gustatory receptors (GRs). The response specificity of these receptor proteins can be deduce using electorphysiological techniques that record the reltative levels of excitation of olfactory receptor neurons (OSNs) residing in various types of sensilla in insect antennae, palps, and tarsi.10. Despite the fact that 50%-90% of plant biomass is underground (the hidden half), it is often neglected in studies of plant life-history, evolution and the ecological interactions between plants and animals. Not surprisingly, these belowground plant parts, namely roots, are diverse in structure, form, and behavior. Living amongst a complex ecological foodweb, roots are often heavily attacked by herbivores and pathogens. Many reviews of plant-insect interactions recognize shortcomings in our ability to evaluate the role of herbivores in shaping natural selection or communities, however, belowground herbivores are only mentioned in passing and the focus is on the visible aboveground communities.11.Improving tolerance and resistance of crop plants to herbivory is key to protecting crop yields, both currently and in future climate change scenarios. Herbivorous insect pests are known to respond to crop plant chemistry, in both the nutrient content of plants and the production of plant defense compounds. Chemotaxis, the chemical attraction or repulsion of insect herbivores to crops, is also dependent upon the volatile organic compounds (VOCs) emitted by the plant.

Progress 07/01/16 to 06/30/21

Outputs
Target Audience:For bumblebees: scientific community, farmers, beekeepers, general public. For fire ants: Scientific community, USDA/APHIS plant protection and quarantinespecialists, general public. For Asian long horned beetle, USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB is threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S.; For mushroom flies (mushroom phorid fly and fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms. For spotted lanternfly: grape growers, tree fruit growers, homeowners in eastern and southeastern Pennsylvania, Pennsylvania hardwood lumber industry. For ground beetles and plants: scientific community, farmers, general public. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?During 2020-21, the project has provided training and professional development for the following personnel: Research Associates/Postdoctoral Researchers:Dr. Michael Wolfin (Postdoctoral Researcher, October 2017-2021, Baker Lab);Dr. Margarita Orlova (Postdoctoral researcher, Jan 2019 - present);Dr. Priscilia Santos (Postdoctoral researcher, March 2020-present); Dr. Chloe Drummond (2018-present, Renner Lab);Dr. Kadeem Gilbert (2019-2021, Renner Lab);Dr. Swayamjit Ray (2016-2020, Ali Lab); Dr. Ching-wen Tan (2019- present, Ali Lab); Dr. Victoria Pocius ( 2018-2020, Ali Lab);Dr. Jessica Kansman (2020-Present, Hermann Lab) Graduate Students:Sonu Koirala B K;Casey Cruse (2020-present, Zhu Lab);Nathan Derstine;Sujay Paranjape;Sarah Spence (2018-present, Amaslem Lab);Adam Rork (2017-present, Renner Lab); Yunjia Liu (2021, Renner Lab);Sujay Paranjape (2021, Renner & Amsalem Labs); Blue Riggins (2021, Renner Lab);Po-An Lin (2017-2021, Felton Lab);Staci Cibotti (2018-present, Ali Lab);Elizabeth Davidson-Lowe (2016-2021, Ali Lab);Kaley Hallmark (2020-present, Ali Lab);Nursyfiqi Zainuddin( 2016- present, Ali Lab); Olivia Trase (2019-present, Ali Lab); Isabella Swyst (2018-present, Ali Lab);Jorge Jaramillo (2021-Present, Hermann Lab);Lillian Germeroth (2020-Present, Hermann Lab) Undergraduate students:Hannah Martin (2019-present, Baker Lab);Ziming He (09/2021-present, Zhu Lab); J. Bagala (2021; Ali-Schilder Lab);E. Luksic (2021; Schilder Lab); K. Rossi (2021; Ali, Schilder & Mongeau labs); H-L. Wu (2021; Ali, Schilder & Mongeau labs); Cameron Murray (Amsalem Lab); Craig, John Maginnis (Amsalem lab); Ian Chamberlain (2020-present, Renner Lab); Shuhan Yin (2021, Renner Lab); Sydney Bird (2019-2020, Hermann Lab); Sophia Mucciolo (2021-Present, Hermann Lab); Jack Thomas (2021-Present, Hermann Lab); Colleen Nersten (2020-Present, Hermann Lab); Megan Czekaj (2021-Present, Hermann Lab) How have the results been disseminated to communities of interest?Presentations by faculty, post-docs and students at a variety of professional meetings reported our progress on our project's goals to University, Industry, and Government researchers. These meetings included the annual meetings of the Entomological Society of America, the International Society of Chemical Ecology,the Ecological Society, Society of Invertebrate Pathology, and at university seminar series and special university invited lectures. A multitude of presentations were made to growers and workers in theagricultural community and to public stakeholders and residents via, for instance, Zoom presentations hosted by the the PennsylvaniaSecretary of Agriculture and the Pennsylvania Department of Agricutlure (PDA). The presentations exhibited our ongoing progress in reducing mushroom phorid fly populations on mushroom farms in S.E. Pennsylvania. Other presentations conveyed our new attract-and-kill technologyfor mushroom phorid fly control to growers at the Annual Mushroom Short Course as well as to workersreceiving pesticide credit training atcourses hosted by the American Mushroom Institute. Our team also presented our research progress atmonthly Zoom meetings during 2020 and 2021of the Phorid Fly Action Committee comprised of concerned residents in S. E. Pennsylvania who are worried about the effects of unbearable mushroom phorid fly invasions of their homes. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? 2. Co-Director Renner:We are working to determine: (1) which genes, among various gene families, are involved in digestive functions and if these genes are homologous to those involved in plant defense, (2) if orthologous gene subfamilies, rather than closely related paralogous gene lineages, been co-opted for digestive functions in independent carnivorous plant lineages, and (3) whether genes that act in prey response are differentially regulated compared to their non-carnivorous paralogs, and if so, by which regulators (e.g., wound-signaling and/or phytohormone cascades). We are also working to understand dietary secondary metabolite production in response to UV, latitude, elevation, and genotype, to assist in targeted plant management. We are: (1) examining the response of secondary metabolite production in thinleaf huckleberry,Vaccinium membranaceum,using controlled treatments of UV intensity, (2) comparing the expression of genes in secondary metabolic pathways and secondary metabolite between low and high elevation populations across a latitudinal gradient, and (3) examining how evolutionary history influences patterns of secondary metabolite production in berries across the geographic range. This work is funded under USDA NIFA PENW-2019-07199 (postdoctoral fellowship to Dr. Chloe Drummond, mentored by Renner). 6. Co-Director Felton To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we showed that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillarHelicoverpa zeaon leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5min, and in both tomato and soybean (Glycine max) for at least 48h. GOX also inhibits the emission of several HIPVs during feeding byH.zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. We found thatP. rapaelarvae experienced higher survival onR. indicagrowing under low water availability compared with plants grown under high water availability. We have also demonstrated in greenhouse studies, that drought conditions decrease the amount of HIPVs released by stressed plants and the subsequent ability of a parasitoid to locate its insect host. Herbivore growth rate increased with temperature, whereas plants growth as well as the ability to tolerate stress measured by photosynthesis recovery and regrowth ability were compromised at the highest temperature regime. 7. Project Director Baker.As part of our new collaboration with a chemical ecology research chemist in Brazil we collected pheromone extract from nearly 1,000 females of the fungus gnat, Lycoriella ingenua, a major pest of cultivated mushrooms around the world. In exhaustive field observations of adult spotted lanternflies, Lycorma delicatula, we definitively characterized the flight-dispersing adults' visual attraction to vertical objects such as telephone poles. They turn toward and land on these objects when they are closer than 2.6 meters away from and more than 3 meters below the top of such a pole. 8. Project Director Baker.We have behaviorally characterized the attraction of the mushroom phorid fly, Megaselia halterata, to the ambient light emanating from the external windows of mushroom-growing rooms in the mushroom houses in SE Pennsylvania. We have used this behavior to successfully kill millions of flies every week using insecticide-laced netting on the windows. 8. Co-Director Myrick.Successful electro-antennograms (EAGs) were performed on a variety of species in our laboratory for the first time. Among these successful EAGs were those performed on bedbugs, aphids, squash bees and its associated parasite bee species, and female monarch butterflies. We used the coupled gas-chromatograph/EAG (GC/EAG) technique such that for the first time we were able to accurately characterize the dose-response profiles of the monarch butterfly's antennal sensitivity. 8. Co-Director Amsalem. We identified and examined the role of several compounds regulating social behavior and reproduction in bumble bees. We showed that old queens produce higher ratio of short to long hydrocarbons compared to young queens, and that these compounds regulate worker reproduction in a context-dependent manner. We further analyzed the composition of the Dufour and labial glands in females and demonstrated their role in regulating worker reproduction (social pheromones), and mating (sex pheromones) and in reflecting female physiology. We further demonstrated the role of brood in regulating female egg laying and gyne production via hunger signals produced by the early larval instars. 9. Co-DirectorAli.We have been quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology. We have been examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarch butterflies, using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism. Recently we have overseen the construction of 30 state-of-the-art monarch flight mills that report all aspects of sustained monarch flight activity to a custom-designed laptop algorithm that can handle all 30 reports at a time. 9. Co-Director Renner:Current projects funded under USDA NIFA PENW-2018-08053 (postdoctoral fellowship to Dr. Kadeem Gilbert, mentored by Renner) examine phylloplane pH regulatory ability in economically important members of the plant orders Malvales (Gossypium and Hibiscus) and Caryophyllales (Beta and Nepenthes), which vary in phylloplane alkalinity and acidity. Specifically, we are studying differential gene expression in leaves actively regulating phylloplane pH utilizing a transcriptomics approach and examining the active microbiome of the leaves using metatranscriptomics. This work advances knowledge of phylloplane pH regulation, which has strong implications for microbial community assembly and thus plant health and growth. 10: Project Director Baker:We have discovered redundant pheromone components emitted by the so-called "E-strain" of the European corn borer moth, Ostrinia nubilalis, that are received by specific odorant receptor proteins (ORs) on the antennae of the males of this species. We showed that the olfactory sensory neurons (OSNs) on the male antennae that express these odorant receptors show excitation to these components and that males respond by flying upwind to the pheromone source when the source emits these previously undiscovered components. 11. Co-Director Ali: We have found numerous cues used by belowground beneficial organisms to locate pests and the specificity of these chemicals for nematode behavior. By analyzing volatile organic compounds from plant roots, pests and different soil context we are gaining insight into ways to increase efficacy of belowground biological control. 12. Co-Director Zhu:In our Spotted Lanternfly project, we analyzed the pesticide residues in flowers, pollen, and honey after treatment of tree of heaven with neonicotinoids. We also investigated the phytochemical levels from spotted lanternflyduring insect development.The bifenthrin potentialdriftfrom Ultra-Low Volume sprayers beyond the target area for SLF and gypsy moth treatment was also evaluated.

Publications

  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Lin, P., Chen, Y., Ponce, G., Acevedo, F., Lynch, J., Anderson, C., Ali, J. and Felton. G. (In Press) Stomata-mediated interactions between plants, herbivores, and the environment. Trends Plant Sci.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Ray, S., Helms, A. M., Matulis, N. L., Davidson-Lowe, E., Grisales, W., & Ali, J. G. (2020). Asymmetry in herbivore effector responses: caterpillar frass effectors reduce performance of a subsequent herbivore. J. Chem. Ecol., 46(1), 76-83.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Tan, C. W., Peiffer, M. L., Ali, J. G., Luthe, D. S., & Felton, G. W. (2020). Top?down effects from parasitoids may mediate plant defence and plant fitness. Funct. Ecol., 34(9), 1767-1778.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Ali, J. G., Casteel, C. L., Mauck, K. E., & Trase, O. (2020). Chemical ecology of multitrophic microbial interactions: plants, insects, microbes and the metabolites that connect them. J. Chem. Ecol., 46(8), 645-648.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Baker TC, Myrick AJ, Wolfin MS, Wang Y (2021) Visual responses of flight-dispersing spotted lanternflies, Lycorma delicatula, toward a tall vertical silhouette in a vineyard. J. Insect Behav. 34:4960.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wanner, K. W., Moore, K., Wei, J., Herdilicka, B. C., Linn, C. E. Jr., and Baker, T. C. (2020) Pheromone odorant receptor responses reveal the presence of a cryptic, redundant sex pheromone component in the European corn Borer, Ostrinia nubilalis. J. Chem. Ecol. 46:567580.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wolfin, M. S., Myrick, A. J., and Baker, T. C. (2020) Flight duration capabilities of dispersing adult spotted lanternflies, Lycorma delicatula. J. Insect Behav. 33: 125-137.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Liu Y, Moural TW, Koirala B K S, Hernandez JA, Shen Z, Alyokhin A, Zhu F. 2021. Structural and functional characterization of one unclassified glutathione S-transferase in xenobiotic adaptation of Leptinotarsa decemlineata. International Journal of Molecular Sciences 22:11921
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Liu Y, Zhu F, Shen Z, Moural T , Li Z, Liu X, Xu H. 2021. Glutaredoxin and thioredoxin peroxidase involved in defense of emamectin benzoate induced oxidative stress in Grapholita molesta. Pesticide Biochemistry and Physiology 176:104881.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Lin, P; Chen, Y; Chaverra-Rodriguez, D; Heu, C; Zainuddin, N; Sidhu, J; Peiffer, M; Tan, C ; Helms, A; Kim, D; Ali, J; Rasgon, J; Lynch, JP; Anderson, C; Felton, G. (2021) Silencing the alarm: An insect salivary enzyme closes plant stomata and inhibits volatile release. New Phytol. 230 (2), 793
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Pingault, L., Varsani, S., Palmer, N., Ray, S., Williams, W.P., Luthe, D.S., Ali, J.G., Sarath, G. and Louis, J., (2021). Transcriptomic and volatile signatures associated with maize defense against corn leaf aphid. BMC Plant Biol., 21(1), pp.1-15.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Adesanya AW, Cardenas A, Walsh DB, Lavine LC, Lavine MD, Zhu F. 2020. RNA interference of NADPH-Cytochrome P450 reductase increases susceptibilities to multiple acaricides in Tetranychus urticae. Pesticide Biochemistry and Physiology 165:104550.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Ban L, Li J, Yan M, Gao Y, Zhang J, Moural TM , Zhu F, Wang X. 2021. Illumina sequencing of 18S/16S rRNA reveals microbial community composition, diversity, and potential pathogens in turfgrass seeds. Plant Disease doi:10.1094/PDIS-06-18-0946-RE
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Orlova, M., Amsalem, E. (2021). Bumble bee queen pheromones are context-dependent Scientific Reports 11 (1), 1-7.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Treanore, E., Barie, K., Derstine, N., Gadebusch, K., Orlova, M., Porter, M. Purnell, F., Amsalem, E. (2021). Optimizing laboratory rearing of a key pollinator, Bombus impatiens. Insects 12 (8), 673.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Derstine, N., Villar, G., Hefetz, A., Millar, J., & Amsalem, E. (2021). Dufours gland analysis reveals caste and physiology specific signals in Bombus impatiens. Sci. Rep. 11 (1), 1-13.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Treanore, E. Amsalem E. (2020). The effect of intrinsic physiological traits on diapause survival and their underlying mechanisms in an annual bee species Bombus impatiens. Conserv. Physiol. 8(1), coaa103.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Amsalem E., (2020). One problem, many solutions: Female reproduction is regulated by chemically diverse pheromones across insects. Adv. Insect Physiol. 59, 131-182.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Gilbert, K. & Renner, T. (2021). Acid or base? How do plants regulate the ecology of their phylloplane? AoB PLANTS, 13(4), plab032. doi: https://doi.org/10.1093/aobpla/plab032.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Rork, A. M., Xu, S., Attygalle, A., & Renner, T. (2021). Primary metabolism co-opted for defensive chemical production in the carabid beetle, Harpalus pensylvanicus. J. Chem. Ecol. 47,�334349. doi: https://doi.org/10.1007/s10886-021-01253-2.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Breuss, M. W.#, Mamerto, A.#,�Renner, T.,# & Waters, E. R. (2020). The evolution of the mammalian ABCA6-like genes: analysis of phylogenetic, expression and population genetic data reveals complex evolutionary histories.�Gen. Biol. Evol.. doi:�https://doi.org/10.1093/gbe/evaa179.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Albert, V.A., &�Renner, T. Aquatic angiosperm ambiguities answered. (2020).�Nature Plants. doi:�https://doi.org/10.1038/s41477-020-0607-5.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Mason, C. J., Peiffer, M., St Clair, A., Hoover, K., & Felton, G. W. (2021). Concerted impacts of antiherbivore defenses and opportunistic Serratia pathogens on the fall armyworm (Spodoptera frugiperda).�Oecologia, 1-12.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Lin, P. A., Chen, Y., Ponce, G., Acevedo, F. E., Lynch, J. P., Anderson, C. T., ... & Felton, G. W. (2021). Stomata-mediated interactions between plants, herbivores, and the environment.�Trends Plant Sc.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Lin, P. A., Chen, Y., Chaverra?Rodriguez, D., Heu, C. C., Zainuddin, N. B., Sidhu, J. S., ... & Felton, G. W. (2021). Silencing the alarm: an insect salivary enzyme closes plant stomata and inhibits volatile release.� New Phytologist,�230(2), 793.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Lin, P. A., Paudel, S., Afzal, A., Shedd, N. L., & Felton, G. W. (2021). Changes in tolerance and resistance of a plant to insect herbivores under variable water availability.�Environ. Exp. Bot.,�183, 104334.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Mason, C. J., Hoover, K., & Felton, G. W. (2021). Effects of maize (Zea mays) genotypes and microbial sources in shaping fall armyworm (Spodoptera frugiperda) gut bacterial communities.�Sci. Rep.,�11(1), 1-10.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Wang, J., Mason, C. J., Ju, X., Xue, R., Tong, L., Peiffer, M., ... & Felton, G. W. (2021). Parasitoid causes cascading effects on plant-induced defenses mediated through the gut bacteria of host caterpillars.�Front. Microbiol.,�12.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Paudel, S., Lin, P. A., Hoover, K., Felton, G. W., & Rajotte, E. G. (2020). Asymmetric responses to climate change: Temperature differentially alters herbivore salivary elicitor and host plant responses to herbivory.�J.Chem. Ecol.,�46(9), 891-905.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Tan, C. W., Peiffer, M. L., Ali, J. G., Luthe, D. S., & Felton, G. W. (2020). Top?down effects from parasitoids may mediate plant defence and plant fitness.�Funct. Ecol.,�34(9), 1767-1778.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Po-An, L., Peiffer, M., & Felton, G. W. (2020). Induction of defensive proteins in Solanaceae by salivary glucose oxidase of Helicoverpa zea caterpillars and consequences for larval performance.�Arthr.-Plant Interact.,�14(3), 317-325.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Mason, C. J., St. Clair, A., Peiffer, M., Gomez, E., Jones, A. G., Felton, G. W., & Hoover, K. (2020). Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae.�PloS one,�15(3), e0229848.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Hermann S.L., Bird S., Ellis D., & Landis D.A. (2021) Predation risk differentially affects aphid morphotypes: impacts on prey behavior, fecundity and transgenerational dispersal morphology. Oecologia. doi: 10.1007/s00442-021-05037-z
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Binyameen, M., Hamid, A., Afzal, I., Sajjad, M., Azeem, M., Muhammad Zaka, S., Mehmood Sarwar, Z., Ali Shad, S., Baker, T.C., Schlyter, F. (2021) Role of fruit volatiles of different guava varieties in attraction and oviposition behaviors of peach fruit fly, Bactrocera zonata Saunders. Arthro.-Plant Interact. 15:95106.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Davidson-Lowe E, Zainnudin N, Ali JG (2020). Opening a can of worms: Do AMF alter belowground interactions between plants, root herbivores and their natural enemies? Entomology Society of America- Virtual Meeting
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Swyst, I. & Ali, J.G. (2020) Arbuscular mycorrhizal fungi alters soybean resistance against herbivores in a feeding guild specific manner. Entomology Society of America- Virtual Meeting
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Ali, J. (2021) " Chemical ecology of plant defense and multi-trophic interactions: bad bugs, pungent parasites and toxic travelers." University of Virgina, Department of Biology, Charlottesville, VA.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Ali, J. (2021) " Chemical ecology of plant defense and multi-trophic interactions: bad bugs, pungent parasites and toxic travelers." University of Idaho, Entomology, Plant Pathology and Nematology, Moscow, ID.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Ali, J. (2021) " Chemical ecology of plant defense and multi-trophic interactions: bad bugs, pungent parasites and toxic travelers." University of Georgia, Department of Entomology, Athens, GA.
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Hermann S.L. & Thaler J.S. (2021) Chemical ecology and predator-prey interactions: understanding the role of chemistry on complex, trophic relationships in a changing world. J. Chem. Eco.l�47,�819821 (2021).�https://doi.org/10.1007/s10886-021-01328-0
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Baker, T. C., February 4, 2021. South Africa (via Zoom). Visual Responses of Male�Agrilus�spp. to Female Decoys Emitting Different Structural Colors" and Light-Strands. IUFRO Webinar Series: Ecology and Management of Bark and Woodboring Insects.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Baker, T. C., March 24, 2021. Useful Chemical Ecology Research Without the Chemicals . Eastern Branch Entomological Society of America (via Zoom).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Baker, T. C., 2021. International Society for Chemical Ecology, Stellenbosch, South Africa (via Zoom). An OR having previously unrecognized wide-field ligand affinities explains the behavioral activity of a new, cryptic, redundant sex pheromone component in the moth, Ostrinia nubilalis.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Baker, T. C., 2021. Ohio State University OARDC, Wooster, OH. Entomology Departmental Seminar Series. Flight Dispersal Behavior of the Spotted Lanternfly, Lycorma delicatula.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Renner, T. (2021). Reduce, reuse, recycle: whole genome evolution, gene co-option, and convergence among the carnivorous plants, Department of Botany and Plant Pathology Bonnie Templeton Seminar, Oregon State University, Corvallis, OR. Invited. National.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Drummond, C.P. (Presenter), Chamberlain, I.*, & Renner, T. (Presentation on demand, 2021). A case of the blues, reds, and purples: flavonoid biosynthesis and evolution in Vaccinium L. Botany Meeting, Virtual Meeting, International.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Renner, T. (March 12, 2021). Reduce, reuse, recycle: whole genome evolution and gene co-option among the carnivorous plants, Plant Biology Seminar Series, UC Davis, Davis, CA. Invited. National.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Renner, T. (January 23, 2021). Evolution of structural and chemical defense in the carnivorous plants, Winter Meeting, Mid-Atlantic Carnivorous Plant Society, Virtual, Invited. National.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Renner, T. (November 2, 2020). Co-option, convergence, and chemistry: a comparative genomic approach to study the evolution of defense in plants and insects, Entomology Seminar, North Carolina State University, Raleigh, NC, Invited. National.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Renner, T. (October 12, 2020). Co-option, convergence, and chemistry: a comparative genomic approach to study the evolution of defense in plants and insects, School of Biological Sciences Seminar Series, University of Bristol, Bristol, UK, Invited. International.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2021). Where do pollinators go in the winter? stressors affecting bumble bee health during the solitary phase. The Annual meeting of Entomology (ESA), Denver, CO (Invited).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2021). Reproductive signaling in bees. The 36th Annual Meeting of the International Society for Chemical Ecology, Virtual conference (Invited).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2021). Reproductive signaling in bees: The mighty queen, the power of peers and the role of brood. The 58th Annual Conference of the Animal Behavior Society, Virtual conference (Accepted).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2021). Sterility inducing mechanisms in bumble bees. Cramer seminar series, Department of Biological Sciences, Dartmouth College, NH (Invited).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2021). Reproductive signaling in bees: The mighty queen, the power of peers and the role of brood. Biology & Genomics of Social Insects conference in Cold Spring Harbor, Virtual conference (Invited).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2021 Citation: Amsalem, E. (Presenter & Author). (2020). Sterility inducing mechanisms in social insects. IOS CAREER Awardee Conference, Virtual conference (Invited).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Amsalem, E., Barie, K. (Presenter & Author). (2020). A method for the in-vitro rearing of Bombus impatiens brood. The Annual meeting of Entomology (ESA), Virtual conference.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Amsalem, E. Barie K (Presenter & Author). (2020). A method for the in-vitro rearing of Bombus impatiens brood. The 57th Annual Conference of the Animal Behavior Society, Virtual conference.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Amsalem, E. (Presenter & Author). (2020). Diapause in bees. Biology of Winter Gordon Research Conferences, Boston MA. CANCELLED DUE TO COVID-19 (Accepted).


Progress 10/01/19 to 09/30/20

Outputs
Target Audience:For bumblebees: scientific community, farmers, beekeepers, general public For fire ants: Scientific community, United States Department of Agriulture Animal and Plant Health Inspection Service(USDA/APHIS),plant protection and quarantinespecialists, general public For Asian long horned beetle (ALB), USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB is threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S. For mushroom flies (mushroom phorid fly and fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms For spotted lanternfly: grape growers, tree fruit growers, homeowners in eastern and southeastern Pennsylvania, Pennsylvania hardwood lumber industry For ground beetles and plants: scientific community, farmers, general public Changes/Problems:No problems. Some changes include: In 2019-20, the project added a new P.I., Dr. Sara Hermann. She joined the three new P.I.s that were added in 2018-2019: Dr. Ruud Schilder, Dr. Rose Zhu, and Dr. Gary Felton, all of whom joined the project too late in 2018-2019 to contribute to last year's report. For 2019-onward, the previous Goal 12 has been removed and replaced by a new Goal 12 (above), due to the addition of Dr. Rose Zhu to the CRIS-4609 Project. What opportunities for training and professional development has the project provided?During 2019-20, the project has provided training and professional development for the following personnel: Research Associates/Postdoctoral Researchers: 10 Graduate Students: 20 Undergraduate students: 11 Awards and Honors for Graduate Students in 2019-2020: 3 Outreach and Service by Graduate Students: 5 How have the results been disseminated to communities of interest?Presentations by faculty, post-docs and students at a variety of professional meetings such as the annual meetings of the Entomological Society of America, the International Society of Chemical Ecology,the Ecological Society, Society of Invertebrate Pathology, and at university seminar series and special university invited lectures. What do you plan to do during the next reporting period to accomplish the goals?Our group will do our best to prevail during whatever happens with regard to the future course of the COVID-19 pandemic and achieve good progress regardless of the constraints and restrictions that are imposed (by necessity of maintaining good health) by our university. We anticipate continued creative and productive research related to our project during 2020-2021. The Tumlinson lab will completethe identification and synthesis of the small heat-stable effector from caterpillar regurgitant and determine its mode of action to prevent (Z)-3-hexenal as a substrate for further GLV biosynthesis. The lab will further identify genes whose transcription is regulated specifically by GLV in the context of wounding and insect-provided elicitors (Objective 3). During the next reporting peroid, the Zhu lab will continue to investigate xenobiotic adaptation and antioxidant defense mechanisms in several agriculturally important insect pests and beneficial insect species including pollinators. Specifically, we will further reveal the functions of genes/proteins that may play roles in xenobiotic detoxification and regulation of xenobiotic detoxification. We will also continue working with the environmental effects of pesticide applications in pest management on pollinators. The Schilder lab will continue to collaborate with the Ali lab on the Monarch-millkweed project and derivations thereof (e.g., effects of neonicotinoid exposure on plant-herbivore interactions). We will move forward with studies of environmental and dietary impacts on insect locomotor performance and energetics in other model insect systems (e.g., Drosophila flies, Schistocerca locusts, Bombus bumble bees) via classic methodology (e.g., respirometry, flight kinematics) and newly developed neuromechanical control paradigms (e.g., perturbation of optomotor responses in virtual reality settings). The Baker lab will procede to enhance and further develop the continuing lines of research established during this last reporting period. We will develop ways to characterize the stereoisometry of the germacradienol sex pheromone component of the fungus gnat, L. ingenua, using new approaches consisting of chemical derivatives and use of starting materials from the pheromone of another nematoceran fly species to create potentially active derivatives (Objective 10). We will take our investigations further on the visual attraction of spotted lanternfly adults to vertical objects such as telephone poles and try to optimize this behavioral attraction for attract-and-kill purposes as well as the use of telephone poles as visual "traps" that can be effective for monitoring the spread of this pest species during flight dispersal. We will be working to try to use biorational pesticide products to suppress populations of the mushroom phorid fly, M. haltera, in mushroom-growing facilities and will continue to optimize a behavioral bioassay system for confirming the pheromonal activity of two components that have been isolated, identified, and synthesized.

Impacts
What was accomplished under these goals? Objective 2. (Renner) We have extended study of theCephalotus follicularis(Oxalidales),Drosera capensis(Caryophyllales), and Pinguicula sp. (Lamiales) genomes to their own tandemly duplicated gene content, uncovering similar enrichments. Current work combines genomics with experimental transcriptomics to furtherunderstand functional shifts in protein evolution. Research we performed regarding pathogenesis-related (PR) proteins suggests that during the evolution of carnivory within carnivorous plant lineages, chitinase genes primarily utilized for pathogenesis response by ancestral non-carnivorous plants duplicated and diverged. Through subsequent co-option, the chitinases were then subfunctionalized for pathogenic response versus digestion, substantiated by shifts in selection pressures affecting protein structure and function. Objective 4. (Tumlinson) Elicitor-treated maize seedlings, within three-fourhours after treatment, produced higher transcript levels of ZmLOX10 and ZmHPL (requisite for biosynthesis of green leafvolatiles [GLV]) compared to wounded-only seedlings, and even higher when compared to intact seedlings. On the other hand, caterpillars suppress GLV emission by at least three different mechanisms, all of which result in effectively reducing the production of (Z)-3-hexenol by either preventing (Z)-3-hexenal from being synthesized, or shunting it off through isomerization and/or sequestration. Moreover, when caterpillars were allowed to feed for two days on tobacco, we observed higher GLV emissions on the second day of feeding (Timilsena et al. 2020). Taken together, these results suggest that after prolonged feeding elicitor-induced GLV biosynthesis in essence outcompetes the suppression mechanisms of the caterpillar. Objective 6. (Felton) We tested the impact of salivary Glucose Oxidase (GOX) on induction of two common defense proteins, trypsin protease inhibitors (TPI) and polyphenol oxidases (PPO), and on relative growth rate of H. zea. GOX specifically induced TPI activity in tomato and habanero pepper, and the level of defense protein depended on leaf location. Changes in performance in tomato and habanero pepper matched the induction of TPI. Our findings thus indicate that GOX induces similar defense responses in some solanacean plants, but largely depends on species/genotype of plant. We identified five secreted fungi from black cutworm including Aspergillus parasiticus, A. niger, Geotrichum candidum, Fusarium subgltinans, and Mucor circinelloides f. lusitanicus. We found that caterpillars inoculated with F. subglutinans or M. circinelloides f. lusitanicus induced higher defense responses in plants, but with different patterns between different plants. These herbivore-induced defense responses reduced the growth of caterpillars. Our findings suggest that insect-associated fungi could influence plant-insect interactions by indirectly mediating plant defense responses, and directly affecting caterpillar performance on host plants. Objective 7. (Baker & Amsalem) We have developed a new collaboration with a chemical ecology research chemist in Brazil and have developed new strategies in our lab to try to definitively identify and charactierize the stereospecific structure of the sex pheromone of the fungus gnat, Lycoriella ingenua, a major pest of cultivated mushrooms around the world. In exhaustive field observations of adult spotted lanternflies, Lycorma delicatula, we found that flight-dispersing adults tend to orient strongly to objects in the environment that offered a strong visual stimulus in the form of a vertical silhouette, such as lamp posts, tree trunks, and telephone poles. We also found that shorter, "local" plant-to-plant flights can transform into higher-altitude longer range dispersal flights when spurious instances of buoyant air occur in the field, elevating the adults to then be able to drift many hundreds of meters downwind and create longer-distance flight dispersal. In work on the social bumblebee species Bombus impatiens, we found that first and second instar brood regulate egg laying behavior in adult workers. We showed that the brood effect was general and independent of its sex or relatedness to workers. We further examined how the brood communicates its presence by introducing workers to whole body extracts, body washes or volatiles produced by young larvae using a vacuum air-flow system. Objective 8. (Baker & Myrick) Extracts from females of Megaselia halterata, the mushroom phorid fly,revealed that two compounds possibly comprising the sex pheromone were three, 6-dimethylheptane-2,4-dione and its enol form. Synthesis of these compounds was performed by Prof. Tappey Jones of the Virginia Military Institute. Work is proceeding to try to increase the selectivity of a new type of more discriminating assay to confirm the behavioral activity of these two synthetic pheromone components. Objective 9. (Schilder and Ali) We have been quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology. We have been examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarch butterflies, using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism. Recently we have overseen the construction of 30 state-of-the-art monarch flight mills that report all aspects of sustained monarch flight activity to a custom-designed laptop algorithm that can handle all 30 reports at a time. We are conducting long-term studies of the effects of protozoan (single celled eukaryotic pathogens) infections on flight capacity of migratory and non-migratory dragonflies. We are currently examining how environmental factors such as aquatic pH levels interact with the dragonfly microbiome to affect susceptibility to infection. Objective 11. (Ali) We investigated plant and insect responses to chemical cues from below-ground natural enemies and explored the ecological significance of these cues for multitrophic interactions. We examined the influence of odors emitted by entomopathogenic nematodes (EPNs), a natural enemy of insect herbivores, on the performance and behavior of their insect prey and the defense responses of nearby plants. We foundthat EPN-infected insect cadavers emit a characteristic blend of volatile compounds that influences both the performance and preference of a specialist herbivore, Colorado potato beetle (CPB, Leptinotarsa decemlineata), feeding on its host plant, potato (Solanum tuberosum). We have also found that the volatiles emitted by EPN-infested insect cadavers have plant-synthesized performance-reducing effects on herbivore pests. Objective 12. (Zhu) In our Spotted Lanternfly project, we analyzed the pesticide residues in flowers, pollen, and honey after treatment of tree of heaven with neonicotinoids. We identified significant levels of imidacloprid in 15 of 86 honey samples collected from 23 PA counties. The lethal and sublethal effects of imidacloprid residue detected will be further analyzed with bioassay and behavior assays. We have no accomplishments to report for objectives 1, 3, 5, 10.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Albert, V.A. and Renner, T. (2020). Aquatic angiosperm ambiguities answered. Nature Plants. doi: https://doi.org/10.1038/s41477-020-0607-5
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Breuss, M.W., Mamerto, A., Renner, T., and Waters, E.R. (2020). The evolution of the mammalian ABCA6-like genes: analysis of phylogenetic, expression and population genetic data reveals complex evolutionary histories. Genome Biology and Evolution. doi: https://doi.org/10.1093/gbe/evaa179. (#) these authors contributed equally.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Paudel Timilsena, B., Seidl-Adams, I., & Tumlinson, J. H. (2020). Herbivore specific plant volatiles prime neighboring plants for nonspecific defense responses. Plant, Cell & Environment, 43(3), 787800. https://doi.org/10.1111/pce.13688
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Shen Z, Liu Y, Zhu F, Cai L, Liu X-M, Tian Z, Chen J, Li Z, Liu X-X. 2020. MicroRNA-277 regulates dopa decarboxylase to control larval-pupal and pupal-adult metamorphosis of Helicoverpa armigera. Insect Biochemistry and Molecular Biology 122:103391.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: AW, Adesanya Walters T, Lavine MD, Walsh DB, Lavine LC, Zhu F. 2020. Multiple insecticide resistance in onion thrips populations from Western USA. Pesticide Biochemistry and Physiology 165:104553.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Adesanya AW, Cardenas A, Walsh DB, Lavine LC, Lavine MD, Zhu F. 2020. RNA interference of NADPH-Cytochrome P450 reductase increases susceptibilities to multiple acaricides in Tetranychus urticae. Pesticide Biochemistry and Physiology 165:104550.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wu H, Liu Y, Shi X, Zhang X, Ye C, Zhu KY, Zhu F, Zhang J, Ma E. 2020. Transcriptome analysis of antennal cytochrome P450s and their transcriptional responses to plant and locust volatiles in Locusta migratoria. International Journal of Biological Macromolecules 149:741-753.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Jones, A. M., Van de Wyngaerde, M. T., Machtinger, E. T., Rajotte, E. G., and Baker, T. C. (2020) Choice of laboratory tissue homogenizers matters when recovering nucleic acid from medically important ticks. J. Med. Entomol. 57: 12211227.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wanner, K. W., Moore, K., Wei, J., Herdilicka, B. C., Linn, C. E. Jr., and Baker, T. C. (2020) Pheromone odorant receptor responses reveal the presence of a cryptic, redundant sex pheromone component in the European corn Borer, Ostrinia nubilalis. J. Chem. Ecol. 46:567580.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wolfin, M. S., Myrick, A. J., and Baker, T. C. (2020) Flight duration capabilities of dispersing adult spotted lanternflies, Lycorma delicatula. J. Insect Behav. doi.org./10.1007/s 10905-020-09754-w.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Mason, C. J., St. Clair, A., Peiffer, M., Gomez, E., Jones, A. G., Felton G. W., and Hoover, K. (2020) Diet influences proliferation and stability of gut bacterial populations in herbivorous larvae. Plos ONE 15: e0229848.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Tan, C. W., Peiffer, M. L., Ali, J. G., Luthe, D. S., and Felton, G. W. (2020) Top-down effects from parasitoids may mediate plant defence and plant fitness. Funct. Ecol. 34: 17671776.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Lin, P. A., Peiffer, M., and Felton, G. W. (2020) Induction of defensive proteins in Solanaceae by salivary glucose oxidase of Helicoverpa zea caterpillars and consequences for larval performance. Arthropod-Plant Interact. 19.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Chen, X., Peiffer, M., Tan, C. W., and Felton, G. W. (2020) Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plant-insect interactions. Arthropod-Plant Interact. 110.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Orlova, M., Starkey, J. A., & Amsalem, E. (2020) A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee. Journal of Experimental Biology 223 (3).
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Treanore, E. D., Kiner, J. M., Kerner, M. E., & Amsalem, E. (2020). Shift in worker physiology and gene expression pattern from reproductive to diapause-like with colony age in the bumble bee Bombus impatiens. Journal of Experimental Biology 223 (9)
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Adesanya AW, Beauchamp M, Lavine MD, Lavine LC, Zhu F, Walsh DB. 2019. Physiological resistance alters behavioral response of Tetranychus urticae to acaricides. Scientific Reports 9:19308.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Miko, I., Rahman, S. R., Jones, A., Townley, M. A., *Gominho, B., Paudel, S., *Stupski, D., Hines, H. M., Schilder, R. J. (2019). From spinning silk to spreading saliva: mouthpart remodeling in Manduca sexta (Lepidoptera: Sphingidae). Insect Systematics and Diversity (accepted 05/16/19).
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Schilder, R. J., *Stewart, H. (2019). Parasitic gut infection causes functional and molecular resemblance of dragonfly flight muscle to skeletal muscle of obese vertebrates. The Journal of Experimental Biology doi: 10.1242/jeb.18850
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Miko, I., Rahman, S. R., Anzaldo, S., van de Kamp, T., Parslow, B. A., Tatarnic, N. J., Wetherington, M. T., Anderson, J., Schilder, R. J., Ulmer, J. M., Deans, A. R., Hines, H. M. (2019). Fat in the leg: function of the expanded hind leg in gasteruptiid wasps (Hymenoptera: Gasteruptiidae). Insect Systematics and Diversity 3(1): 2.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Jones, A. G., Mason, C. J., Felton, G. W., and Hoover, K. (2019) Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci. Rep. 9:111.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mason, C. J., Jones, A. G., and Felton, G. W. (2019) C-option of microbial associates by insects and their impact on plant-folivore interactions. Plant, Cell & Environ. 42: 10781086.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mason, C. J., Ray, S., Shikano, I., Peiffer, M., Jones, A. G., Luthe, D. S., and Felton G. W. (2019) Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proc. Nat. Acad. Sci. (U.S.) 116: 1599115996.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Acevedo, F. E., Smith, P., Peiffer, M., Helms, A., Tooker, J., and Felton, G. W. (2019) Phytohormones in fall armyworm saliva modulate defense responses in plants. J. Chem. Ecol. 45:598609.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Renner, T. (October 12, 2020). "Co-option, convergence, and chemistry: a comparative genomic approach to study the evolution of defense in plants and insects, University of Bristol, Bristol, England, Invited. International
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Renner, T. (August 26, 2020). Carabids, chemistry, and convergence: utilizing comparative genomics to study the evolution of chemical defense in ground beetles, Purdue University, West Lafayette, Indiana, Invited. National.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Fleck, S. J., Nolan, K., Bocklund, K., Lan, T., Tomlin, C., Ibarra-Lacletee, E., Rosas, M. M., Michael, T., Renner, T., & Albert, V. A. (January 11, 2020 - January 15, 2020). "Preliminary Genome Assemblies of Butterworts (Pinguicula, Lentibulariaceae) suggest both Divergent and Convergent Evolution of Genomic Features Important in Prey Digestion," Plant and Animal Genome Conference XXVIII, San Diego, CA, Accepted. International.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Albert, V., Abramson, B., Cho, N., Fleck, S. J., Fukushima, K., Hartwick, N., Khew, G., Lindqvist, C., Low, Y. W., Michael, T., Nolan, K., Rajaraman, S., Renner, T. (Author Only), Saloj�rvi, J., Saul, F., Scharmann, M., & Tomlin, C. (January 12, 2020). "Sequencing and Assembling Highly Heterozygous and/or Repeat-Rich Plant Genomes using Oxford Nanopore Technology," Plant and Animal Genome Conference XXVIII, San Diego, CA, Accepted. International.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Renner, T. (Presenter & Author), Rork, A. M., McManus, R. B., Gill, A. S., Xu, S., Will, K., Attygalle, A., & Moore, W. (November 19, 2019). "A comparative genomic approach for studying the evolution of carabid beetle defensive chemistry," Entomology 2019, The Entomological Society of America, St. Louis, MO, Accepted. International.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Rork, A. M., Xu, S., Attygalle, A., & Renner, T. (Author Only). (November 18, 2019). "Primary metabolism co-opted for defensive chemical production in the carabid beetle, Harpalus pensylvanicus," Entomology 2019, The Entomological Society of America, St. Louis, MO, Accepted. International.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Renner, T (Presenter & Author). (October 2019). "Co-option, convergence, and chemistry: a comparative genomic approach to study the evolution of defense in plants and insects, Cornell University, Ithaca, NY, Invited. Regional.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Moural, T.W., Phan, N., Rajotte, E., Biddinger, D., and Zhu, F. Mechanisms of comparative pesticide toxicities in bees. Invited postdoc talk: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Adesanya, A.W., Walsh, D., Lavine, L., and Zhu, F. RNA interference of NADPH-Cytochrome P450 reductase increases susceptibilities to multiple acaricides in Tetranychus urticae. Invited student talk: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Biddinger, D., Leach, H., Zhu, F., Urban, J.M., and Hajek, A.E. Controlling Spotted lanternfly with insecticides and biopesticides in fruit crops and possible impacts pollinators and other non-target insects. Invited talk: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Hernandez, J., Moural, T.W., and Zhu, F. Characterize a serine protease inhibitor in the Colorado potato beetle. Student presentation: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Zhu, F., Moural, T., and Cao, C. Regulation of xenobiotic detoxification in Lymantria dispar. Oral presentation: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Adesanya, A., Lavine, L., Zhu, F., and Walsh, D. Transcriptional plasticity of a generalist herbivore in adaptation to mite growth inhibitors. Student presentation: Annual Meeting of ESA, St. Louis, MO. November, 2019.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Environmental impacts of pesticides used for Spotted Lanternfly control. Student presentation: 2020 Virtual S.T.E.M. SHOWCASE, Penn State. May, 2020.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Schilder, R. (November 2019). "Factors mediating naturally occurring variation in insect flight (muscle) performance." School of Biological Sciences, University of Nebraska, Lincoln, NE.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Schilder, R. (November 2019). "Factors mediating naturally occurring variation in insect flight (muscle) performance." Department of Zoology and Physiology, University of Wyoming, Laramie, WY. rescheduled due to COVID-19.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Stewart, H., Schilder, R. (November 2019). "The cost of immune responses to thermoregulatory capacity in Bombus impatiens bumble bees." Entomological Society of America Annual Meeting, St. Louis, MO, USA.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Stewart, H., Schilder, R. (October 2019). "Trade-offs between thermoregulatory strategies and immunocompetence in the bumblebee Bombus impatiens." BOMBUSS 2.0, Toronto, ON, Canada.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Baker, T. C. October 29, 2019. Biglerville, PA Spotted lanternfly working group conference. Flight dispersal capabilities of female SLF related to size and mating." Invited.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Baker, T. C.. November 8, 2019. Princeton University. Princeton, NJ. Neuroethology of insect olfaction." Invited.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Baker, T.C.. November 20, 2019. St. Louis, MO. Entomological Society of America annual meeting. Invited symposium speaker. What we know so far about how feeding and mating are related to Lycorma delicatula flight dispersal behavior." Invited.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "Social evolution in bees: insights gained from studying evolution of advanced eusocial traits." The Annual meeting of Entomology (ESA), Saint Louis, MO (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "Conservation Physiology: Helping bumble bees thrive." BOMBUSS 2.0 conference, Toronto, Canada (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "Do bumble bees (Bombus impatiens) produce brood pheromone?" The 35th Annual Meeting of the International Society for Chemical Ecology, Atlanta, GE (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "Mechanisms and evolution of insect social behavior and applications to pollinator health. Seminar, Department of Ecology, Evolution and Behavior, The Hebrew University, Jerusalem, Israel (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "The road to sociality in insects: Mechanisms and evolution." Faculty research talks for incoming Molecular Cellular and Integrative Biosciences (MCIBS) students, University Park, PA (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "The road to sociality in insects: Mechanisms, evolution and applications to pollinator health." Seminar, Department of Entomology, University of Arizona, Tucson, AZ. (Invited).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2019 Citation: Amsalem, E. (Presenter & Author). (2019). "The road to sociality: Brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens." The 56th Annual Conference of the Animal Behavior Society and the 36th International Ethological Conference, Chicago, IL (Accepted).
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Amsalem, E., Barie, K. (Presenter & Author). (2020). A method for the in-vitro rearing of Bombus impatiens brood. The Annual meeting of Entomology (ESA), Virtual conference (Accepted)
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Amsalem, E. Barie K (Presenter & Author). (2020). A method for the in-vitro rearing of Bombus impatiens brood. The 57th Annual Conference of the Animal Behavior Society, Virtual conference, (Accepted)
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2020 Citation: Amsalem, E. (Presenter & Author). (2020). Diapause in bees. Biology of Winter Gordon Research Conferences, Boston MA. Cancelled due to COVID- 19.


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:For bumblebees: scientific community, farmers, beekeepers, general public. For fire ants: Scientific community, USDA/APHIS plant protection and quarantine specialists, general public. For Asian long horned beetle, USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB is threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S. For mushroom flies (mushroom phorid fly and fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms. For spotted lanternfly: grape growers, tree fruit growers, homeowners in eastern and southeastern Pennsylvania, Pennsylvania hardwood lumber industry. For ground beetles and plants: scientific community, farmers, general public. Changes/Problems:During this reporting year, we intiaited a new Goal;Goal 12 - Unravel the mechanisms that allow specific cover crops to foster resistance against insect pests via arbuscular mycorrhizal fungi associations. Cover crop species farmers choose has legacy effects on the subsequent corn crop's resistance to European corn borer that is mediated by soil fertility and/or mycorrhizal colonization. What opportunities for training and professional development has the project provided?During 2018-19 the project has provided training and professional development for the following personnel: Research Associates/Postdoctoral Researchers: Dr. Kadeem Gilbert (USDA-NIFA postdoctoral fellow, Renner Lab, 09/2019-current) Dr. Chloe Drummond (Postdoc, Renner Lab, 08/2018-current) Dr. Margarita Orlova (Jan 2019 - present) - Postdoc Dr. Irmgard Seidl-Adams Dr. Andrew Myrick Dr. Michael Wolfin Dr. Gabriel Villar Dr. Anjel Helms ( USDA Fellow) Dr. Swayamjit Ray Dr. Timothy Moural Graduate Students: Adam Rork Katie Nolan Nathan Derstine Erin Treanore Arash Maleki Anne Jones Bipana P. Timilsena Tristan Cofer Jesse Starkey Adam Damon Elizabeth Davidson-Lowe Nursyafiqi Zainuddin Erin Treanore (August 2017 - Present) - PhD Nathan Derstine (August 2018 - Present) - PhD Sean Bresnahan (PhD, MCIBS rotation student) Katherine Barie (PhD) Jonathan Hernandez Yanjun Liu Undergraduate students: Arthi Bala (Renner Lab, 08/2018-current) Mark Porter (Renner Lab, 08/2018-05/2019) Jacklyn Kiner (1/2018 - current) Fredrick Purnell (8/2017 - current) Monique S. Porter (Honor Student) Kaitlin M. Gadebusch Ahja Brown (3-12/2017) In addition, 4 undergraduate students have assisted with experiments in the Tumlinson lab and thus gained research experience. Further, through Penn States SROP a student from Virginia State University gained research experience in the Tumlinson lab. How have the results been disseminated to communities of interest?Various Invited Seminars, Presentations at Scholarly/Scientific Meetings - see products listing What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period Amsalem's lab will continue working on the evolution of ester sterility signal in bees and the brood pheromone in bumblebees. The lab will isolate and identify components of the above pheromones and examine their effect on different aspects related to worker reproduction, colony productivity and social organization. The lab will also investigate the genetic underlying the biosynthesis of Dufour gland esters, and the brain gene expression in response to brood and queen presence in Bombus impatiens. Work will begin on a new collaboration aiming at understanding the synergetic effect of queen behavior and the production of fertility signals on worker reproduction, and whether these queen signals are context dependent. Efforts will be made to identify these co-occurring effects during the transitions of queens between major life cycle events such as mating, colony founding, and during the competition phase, during which the queen is active, yet, no longer able to inhibit worker reproduction. The Tumlinson lab will study the emission of green leaf volatiles (GLV) by plants in response to insect herbivory. The lab will also investigate the mechanisms by which insect herbivore-produced compounds modify GLV production and/or emission by plants. A second project will focus on priming of plant defenses by volatile organic compounds (VOC) from herbivore damaged plants. Target plants will include maize and tobacco. Insect herbivores studied will include Spodoptera exigua, Manduca sexta, Trichoplusia ni and Heliothis virescens. The Tumlinson lab will isolate and identify components of herbivore oral secretions that inhibit and/or modify GLV production and emission. During the next reporting period the Baker lab will continue to try to completely characterize the stereochemical structure of the germacradienol compound we isolated from the sciarid fly fungus gnat, Lycoriella ingenua. The lab will try to complete the isolation and identification of the sex pheromone of the phorid fly mushroom pest, Megaselia halterata by conducting definitive behavioral bioassays of the two synthesized putative pheromone components. The Ali lab will continue during the next reporting period to work on plant toxicity consequences on monarch migration. The lab iwill also further characterize the compounds that are emitted from nematode-infested cadavers to understand the precise blend ratios of molecules required to increase plant resistance. Additional crop species will be tested for enhanced pest resistance after exposure to these compounds. Work will proceed during the next reporting period in employing behavioral assays for insect choice among plants grown following various cover-crop plants and learning more about any differences in different plant species' ability to distinguish plants having high beneficial microbial communities. In greenhouse and field experiments the Ali lab will evaluate how three cover crop species affect crop plant resistance. We will monitor mycorrhizal colonization, corn chemical response, corn resistance to both above- and belowground pests, and their behavior. In addition, the Ali lab will begin working on a new project investigating the impact of spotted lanternfly on the quality of Pennsylvania wines. During the next reporting period, the Renner lab will continue to study the genes responsible for the biosynthesis of ground beetle chemical compounds. Specifically, the lab is interested in (1) whether distantly-related species that produce the same compounds are using the same gene family members, (2) what variation exists at the molecular level, and (3) whether genes involved in biosynthesis have been co-opted from those used in general metabolic processes. The Renner lab will also continue to study the interface between plant nutrient acquisition and defense using carnivorous plants as model organisms. The lab is particularly interested in whether whole genome or tandem duplications are responsible for the prevalence of genes involved in essential nutrient assimilation and deterrence of insect herbivores/pathogenic microorganisms, and to study this, we will continue to use new methods in long-read sequencing to assemble high-quality genomes. In addition, we are interested in whether after a gene duplication event, regulatory divergence in gene expression and function occurs. To determine the degree of cross-talk between the regulation of genes involved in nutrient acquisition and defense, we will apply various nitrogenous substrates and phytohormones to plants in vitro and measure gene expression using methods in comparative transcriptomics. The Zhu lab will continue to investigate chemical adaptation mechanisms in several agriculturally important insect pests and beneficial insect species including pollinators. Specially we are interested in revealing the functions of genes/proteins that may play roles in xenobiotic detoxification and regulation of xenobiotic detoxification. We will also start to work with the environmental effects of pesticide applications in pest management on pollinators.

Impacts
What was accomplished under these goals? ? Goals 1, 3, 5, and 6: We report no results this year. Goal 2: Research on pathogenesis-related (PR) proteins suggests that during the evolution of carnivory within carnivorous plant lineages, chitinase genes used for pathogenesis response by ancestral non-carnivorous plants duplicated and diverged. Chitinases were then subfunctionalized for pathogenic response versus digestion, substantiated by shifts in selection pressures affecting protein structure and function. OurUtricularia gibba(Lamiales) work revealed large expansions of defense-related gene families, in addition to genes involved in nutrient acquisition and stress response. Among these, tandem arrays of cysteine protease genes with trap-specific expression evolved within a protein family involved in carnivory in other species. The cysteine protease gene family includes papains thought to have evolved as part of protection from herbivorous insects. Genome analysis of Cephalotus follicularis(Oxalidales),Drosera capensis(Caryophyllales), and Pinguicula sp. (Lamiales) uncovered similar enrichments in tandemly duplicated genes. Goal 4: Caterpillar regurgitant contains two enzymes and one heat-stable small molecule, each of which modifies GLV emission in a different manner. We have isolated and partially purified the small molecule and are conducting experiments to determine its structure. Goal 7: In field work during 2018/19 on Lycorma deliculata, the spotted lanternfly (Hemiptera: Fulgoridae), we found that during their flight dispersal behavior the adults launch themselves upwind to traverse ca. 30-50 meters in single flight-bouts, which are repeated until a new food source is located. Flight capabilities of unmated vs. mated L. delicatula females were assessed to determine the relative threat posed by each type with regard to expanding the infestation area through natural flight behaviors. Mating status was determined for females. Sedentary females on plants were capable of only flying ~4 m when forcibly launched and were significantly heavier than the in-flight-captured females. More than 93% of these large, sedentary females had mated whereas <5% of the flight-captured females had mated. Spontaneously flying females weighed significantly less and had significantly smaller and less yellowed abdomens than sedentary plant-captured females. Nearly all the observed spontaneously flying L. delicatula females were unmated, posing a lower threat to spread the infestation. Goal 8: We have isolated electrophysiologically active compounds from extracts of female mushroom phorid flies, Megaselia halterata to identify the sex pheromone as a strategy to divert flies from mushroom growing areas with synthetic pheromones. Extracts revealed the presence of four electroantennographically (EAG) active compounds: 3, 6-dimethylheptane-2,4-dione and its enol as well as novel diastereomers of the ketol 3,6-dimethyl-2-hydroxyheptane-4-one. We have developed a behavioral bioassay system for flies that showed the two ketols represent the active sex pheromone blend of this species. When presented with the 3:1 blend of these two compounds, male flies responded with significant flight activity. Pheromones regulating cooperative behavior and social organization in insect societies are one of the supreme puzzles in social evolution. First and second instar brood of social bumblebee species Bombus impatiens regulate egg laying behavior in adult workers. Brood effect was general and independent of its sex or relatedness to workers. We examined how the brood communicates its presence by introducing workers to whole body extracts, body washes or volatiles produced by young larvae using a vacuum air-flow system. None of these extracts were able to replicate the full effect of live brood. Young brood and the queen regulate distinct genetic pathways in worker's brain, suggesting that their inhibitory effects are complimentary. In the evolution of Dufour gland produced esters in bees, we examined the transition in the role of esters from purely functional in solitary bees to a communicative role signaling reproductive status in social insects. We identified and quantified the production of esters as function of the social and reproductive condition in Bombus (social) and Osmia (solitary) females. Behavioral and electroantennographic bioassays of female perception and attraction to their own Dufour gland have demonstrated attraction in Bombus but not in Osmia bees. In fire ant, Solenopsis invicta, two missing genes in one of the variants of the social chromosome of workers may regulate social organization. Fire ant colonies are headed by either a single queen carrying a homozygote variant of the 'social chromosome' (BB) or by multiple queens carrying the heterozygote variant (Bb). Each of these haplotypes is associated with a particular odor, presumably produced and secreted onto the queen cuticle, allowing the workers to accept or reject queens based on their genotype/odor. Deletion of two genes in the genome of heterozygote workers carrying haplotype b, identified them as odorant receptors that are regulated at the DNA and RNA levels. A bioassay was developed to discriminate queens based on their genotype and reproductive status, and a non-intrusive method to examine the effect of specific genes on social structure. To identify the genes responsible for the biosynthesis of over 250 compounds produced by members of the ground beetle lineage, we have RNA-sequenced the pygidial gland system of Brachinus elongatulus (bombardier beetle) and Harpalus pensylvanicus (PA ground beetle). Genes were identified with putative functions in the biosynthesis of quinones and formic acid. Studying the morphology of tissues responsible production of these chemicals revealed resilin in an insect glandular duct system, which may serve to manage pressure generated by reservoir pump contraction and prevent autointoxification. Goal 9: Variation in milkweed defense biochemistry is linked to variation in larval and adult monarch butterfly fitness traits. Quantifying variation in plant toxicity traits within and across milkweed species has helped us determine how plant defense affects larval growth and subsequent adult fecundity in reproductively active monarch butterfly cohorts. Milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs is being examined using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism. Monarch flight mills report all aspects of sustained monarch flight activity to a custom-designed laptop algorithm. Goal 10: Physiological functions of G-protein-coupled receptors (GPCRs) deduced from the transcriptome of the gypsy moth, Lymantria dispar, is providing insights into how these GPCRs are associated with tolerance to insecticide stresses and involved in the regulation of downstream environmental response genes. GPCRs comprise one of the largest and most diverse family of membrane proteins, which transduce extracellular signals into cellular responses to hormones, neurotransmitters, and environmental stimulants. The ligands of GPCRs are extremely diverse. Ligand binding triggers GPCRs conformational changes activating complex cytosolic signalling networks and causing the intracellular responses. GPCRs play various important roles in modulating sense of vision, smell and taste, immune system and autonomic nervous system. Goal 11: We have found in our project concerning entomopathogenic nematodes (EPNs) that EPN-infested insect cadavers emit volatile compounds, and these indirect chemical cues have plant-synthesized performance-reducing effects on herbivore pests. We are investigating the influence of EPN chemical cues on plants and insect herbivores.

Publications

  • Type: Journal Articles Status: Other Year Published: 2019 Citation: Cloonan, K., Andreadis, S. and Baker, T.C. (2019) Little effect of delayed mating on fecundity or fertility of female fungus gnats, Lycoriella ingenua. Physiol. Entomol. 44: 60-64.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Myrick, A. J. and Baker, T. C. (2019) Analysis of anemotactic flight tendencies of the spotted lanternfly (Lycorma delicatula) during the 2017 mass dispersal flights in Pennsylvania. J. Insect Behav. htttps://doi.org/10.1007/s10905-019-09708-x
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mazin, M., S. S. Andreadis, N. E. Jenkins, K.R. Cloonan, T. C. Baker and E.G. Rajotte (2019) Activity and distribution of the mushroom phorid fly, Megaselia halterata, in and around commercial mushroom farms. Entomol. Exp. Appl. (DOI) - 10.1111/eea.12777.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Baker, T. C., Smyers, E. C., Urban, J. M., Meng,, Z., Pagadala Damadaram, K. J., Myrick, A. J., Cooperband, M. F., and Domingue, M. J. (2019) Progression of seasonal activities of adults of the spotted lanternfly, Lycorma delicatula, during the 2017 season of mass flight dispersal behavior in eastern Pennsylvania. J. Asia-Pac. Entomol. 22:705-713.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Hall, L. P., Graves, F., Myrick, A., Hoover, K., and Baker, T. C. (2019) Labial and maxillary palp recordings of the Asian longhorned beetle, Anoplophora glabripennis, reveal olfactory and hygroreceptive capabilities. J. Insect Physiol. 117: 103905.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Wolfin, M. S., Binyameen, M., Wang, Y., Urban, J. M., Roberts, D. C., and Baker, T. C. (2019) Flight dispersal capabilities of female spotted lanternflies (Lycorma delicatula) related to size and mating status. J. Insect Behav. https://doi.org/10.1007/s10905-019-09724-x.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Cao C, Sun L, Du H, Moural TW, Bai H, Liu P, Zhu F. 2019. Physiological functions of a methuselah-like G protein coupled receptor in Lymantria dispar Linnaeus. Pesticide Biochemistry and Physiology160:1-10.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Sun L, Liu P, Zhang C, Du H, Wang Z, Moural TW, Zhu F, Cao C. 2019. Ocular albinism type 1 (OA1) regulates deltamethrin tolerance in Lymantria dispar and Drosophila melanogaster. Frontiers in Physiology 10, 766
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Domingue, M. J., and Baker, T. C. (2019) Orientation of flight for physically disturbed spotted lanternflies, Lycorma delicatula, (Hemiptera, Fulgoridae). J. Asia-Pac. Entomol. 22: 117-120.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Huang K, Chen W, Zhu F, Li PW, Kapahi P, Bai H. 2019. Ribo-Tag translatomic profiling of Drosophila oenocytes under aging and induced oxidative stress. BMC Genomics 20:50
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Wu M, Adesanya AW, Morales MA, Walsh D, Lavine L, Lavine M, Zhu F. 2019. Multiple acaricides resistance and underlying mechanisms in Tetranychus urticae on hops. Journal of Pest Science 92:543-555.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Adesanya AW, Franco E, Walsh DB, Lavine MD, Lavine LC, Zhu F. 2018. Phenotypic and genotypic plasticity of acaricide resistance in populations of Tetranychus urticae (Acari: Tetranychidae) on peppermint and silage corn in the Pacific Northwest.Journal of Economic Entomology 111:2831-2843.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Tristan M. Cofer, Irmgard Seidl-Adams, and James H. Tumlinson (2018) From Acetoin to (Z)-3-Hexen-1-ol: The Diversity of Volatile Organic Compounds that Induce Plant Responses J. Agric. Food Chem., 2018, 66 (43), pp 1119711208.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Anne C Jones Irmgard Seidl-Adams Jurgen Engelberth Charles T Hunter Hans Alborn James H Tumlinson (2019) Herbivorous Caterpillars Can Utilize Three Mechanisms to Alter Green Leaf Volatile Emission Environmental Entomology, nvy191, https://doi.org/10.1093/ee/nvy191
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Starkey J, Derstine N, Amsalem E. (2019) Do bumblebees produce brood pheromone? (Accepted, Journal of Chemical Ecology, 45(9), 725-734
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Orlova M & Amsalem E. (2019) Context matters: plasticity in response to pheromones regulating reproduction and collective behavior in social Hymenoptera (Current Opinion in Insect Science 35: 69-76)
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Starkey J, Brown A, Amsalem E. (2019) The road to sociality: Brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens (Animal Behavior 154, 57-65)
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Cohanim AB, Amsalem E, Saad R, Shoemaker DD, & Privman E. (2018) Molecular adaptation in olfactory functions on the fire ant social chromosome. Genome biology and evolution 10 (11), 2947-2960
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Rork, A.M., Mik�, I., Renner T. Pygidial glands of Harpalus pensylvanicus (Coleoptera: Carabidae) contain resilin-rich structures. Arthropod Structure & Development. doi: https://doi.org/10.1016/j.asd.2018.12.004. Picked up by news sources (including Penn State News) & featured on the National Science Foundations News Page!
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Rork, A.M., Renner T. Carabidae semiochemistry: current and future directions. 2018. Journal of Chemical Ecology. doi: doi.org/10.1007/s10886-018-1011-8.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Paudel, S., Lin, P. A., Foolad, M. R., Ali, J. G., Rajotte, E. G., & Felton, G. W. (2019). Induced Plant Defenses Against Herbivory in Cultivated and Wild Tomato. Journal of chemical ecology, 45(8), 693-707.
  • Type: Books Status: Published Year Published: 2018 Citation: Matusikova, I., Pavlovic, A., & Renner, T. (Co- Author, 33%), et al. (2018). Biochemistry of Prey Digestion and Nutrient Absorption in Aaron M. Ellison & Lubomir Adamec (Eds.), Carnivorous Plants: Physiology, Ecology, and Evolution. (1st ed.1), (pp. 207-220). Oxford, OX2 6DP: Oxford University Press. Peer-reviewed/refereed. http://global.oup.com/academic/product/carnivorous-plants-9780198779841?cc=us&lang=en&. ISBN/ISSN #/Case #/DOI #: ISBN 978-0-19-877984-1 (hbk.)/DOI 10.1093/oso/9780198779841.001.0001
  • Type: Books Status: Published Year Published: 2018 Citation: Renner, T. (Co- Author, 40%), Lan, T., Farr, K. M., Ibarra-Laclette, E., Schuster, S. C., Hasebe, M., Fukushima, K., & Albert, V. A. (2018). Carnivorous Plant Genomes in Aaron M. Ellison & Lubomir Adamec (Eds.), Carnivorous Plants: Physiology, Ecology, and Evolution. (1st ed.1), (pp. 135-153). Oxford, OX2 6DP: Oxford University Press. Peer-reviewed/refereed. http://global.oup.com/academic/product/carnivorous-plants-9780198779841?cc=us&lang=en&. ISBN/ISSN #/Case #/DOI #: ISBN 978-0-19-877984-1 (hbk.)/DOI 10.1093/oso/9780198779841.001.0001.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Helms, A. M., Ray, S., Matulis, N. L., Kuzemchak, M. C., Grisales, W., Tooker, J. F., & Ali, J. G. (2019). Chemical cues linked to risk: Cues from below?ground natural enemies enhance plant defences and influence herbivore behaviour and performance. Functional Ecology, 33(5), 798-808.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Stelinski, L. L., Willett, D., Rivera, M. J., & Ali, J. G. (2019). Tuningcommunication among four trophic levels of the root biome to facilitate biological control. Biological control.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Markovic, D., Colzi, I., Taiti, C., Ray, S., Scalone, R., Ali, J.G., ... & Ninkovic, V. (2018). Airborne signals synchronize the defenses of neighboring plants in response to touch. Journal of experimental botany, 70(2), 691-700.


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:For bumblebees: scientific community, farmers, beekeepers, general public. For fire ants: Scientific community, USDA/APHIS plant protection and quarantine specialists, general public. For Asian long horned beetle, USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB is threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S.; For mushroom flies (mushroom phorid fly and fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms. For spotted lanternfly: grape growers, tree fruit growers, homeowners in eastern and southeastern Pennsylvania, Pennsylvania hardwood lumber industry. For ground beetles and plants: scientific community, farmers, general public. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?During 2017-18 the project has provided training and professional development for the following personnel: Research Associates/Postdoctoral Researchers: Dr. Chloe Drummond (Postdoc, Renner Lab, 08/2018-current) Dr. Margarita Orlova (will join on January 2019) Dr. Irmgard Seidl-Adams Dr. Andrew Myrick Dr. Kevin Cloonan Dr. Gabriel Villar Dr. Anjel Helms ( USDA Fellow) Dr. Swayamjit Ray Graduate Students: Adam Rork Katie Nolan Nathan Derstine Erin Treanore Arash Maleki Anne Jones Loyal Hall (received PhD in June 2018) Bipana P. Timilsena Tristan Cofer Jesse Starkey Adam Damon Elizabeth Davidson-Lowe Nursyafiqi Zainuddin Undergraduate students: Arthi Bala (Renner Lab, 08/2018-current) Mark Porter (Renner Lab, 08/2018-current) Jacklyn Kiner (1/2018 - current) Fredrick Purnell (8/2017 - current) Ahja Brown (3-12/2017) Mackenzie Kerner (11/2016-5/2017) In addition, 4 undergraduate students have assisted with experiments in the Tumlinson lab and thus gained research experience. Further, through Penn States SROP a student from Virginia State University gained research experience in the Tumlinson lab. Awards and Honors for Graduate Students in 2017-18: Anne Jones: USDA/NIFA Predoctoral Fellowship Grant, 2 Yrs; 2018-2020 Adam Rork: University Graduate Fellowship Erin Treanore College of Agricultural Sciences Travel Award Jesse Starkey College of Agricultural Sciences Travel Award Outreach and Service by Graduate Students: Adam Rork, Katie Nolan (2017/2018) The Great Insect Fair, Department of Entomology (development of two booths: 'Centre Country Carnivores' and 'Amazing Adaptations'. Adam Rork, Katie Nolan (2018) Think Outside the Beaker outreach event with Bellefonte area school district, Eberly College of Science. Adam Rork (2017) Haunted-U outreach event with Centre County area school districts, Eberly College of Science. Gabriel Villar, Jesse Starkey, Nathan Derstine, Erin Treanore, Jacklyn Kiner, Fredrick Purnell (September 2018) The Great Insect Fair (volunteers) Department of Entomology, Penn State Erin Treanore (August 2018) Kids Workshop: Bugs! In the Rohrbach Farm, Catawissa, PA Gabriel Villar, Jesse Starkey, Erin Treanore (July 2018) two days module about chemical communication and social behavior in the Upward Bound Program, Penn State Helms, A.M., Ray, S., Matulis, N.*, Kuzemchak, M.*, Grisales, W.*, Ali, J.G. (February 2018) Chemicalcues from beneficial entomopathogenic nematodes enhance plant protection against herbivores. Poster presentation. Gordon Research Conference and Seminar Plant Volatiles. Lucca, Italy. Ray, S., Helms, A., Matulis, N., Felton, G., Luthe, D. S., & Ali, J. (November 2017). "Chitinases in caterpillar frass alter plant volatile profiles and influence performance of a subsequent herbivore.," Entomology Society of America, Denver, Co. Grisales, W*., Helms, A.M., Ray, S., Ali, J.G. (August 2017) "Investigating Plant responses to indole emitted by entombathogenic nematodes." Poster presentation. The Pennsylvania State University Postdoctoral Society Research Exhibition. University Park, PA. Undergraduate How have the results been disseminated to communities of interest?Amsalem: 1. July 2018, Guarujá, Brazil. Talk in the International conference for the study of social insects (IUSSI): The origin of castes in social insects: Examining the diapause ground plan hypothesis in bumblebees. 2. November 2017, Denver, Colorado. Invited talk in Annual meeting of the Entomological society of America. Regulation of reproductive division of labor in bumble bees - a solved puzzle or an ongoing mystery? Baker 1. November 5, 2017. Denver Colorado. Annual Meeting of the Entomological Society of America. Two symposium presentations: "Sex Pheromone-Mediated Behavior of European Corn Borer Moths: From Strains to Rare Males"; and "Sex Pheromone Olfactory Pathways Related to Pheromone-mediated Behavior of the European Corn Borer" 2. January 11, 2018 - Annapolis, MD - USDA Joint Research Forum on Invasive Species. Lecture entitled, "Spotted Lanternfly Adult Behavior Project - 2017" 3. June 2 - June 16, 2018 -Northeast Forestry University, Harbin China. Presented 12 3-hour lectures in Insect Chemical Ecology to 18 graduate students. 4. June 21, 2018 - Alnarp, Sweden. ICE-18, Insect Chemical Ecology Short Course. Presented a 1.5 hr lecture entitled "Successes in Using Insect Pheromones in Insect IPM Programs". 5. August 14, 2018 - Budapest, Hungary - International Society of Chemical Ecology annual meeting: "Flight Dispersal Behavior of the Invasive Pest Species, Lycorma delicatula (Hemiptera: Fulgoridae)". 6. October 8, 2018 - Riverside, CA - Invited seminar in the Department of Entomology at the University of California, Riverside. "Feeding, Mating, and Flight Dispersal Behavior of the Invasive Pest Species, Lycorma delicatula (Hemiptera: Fulgoridae)". Ali 1. Ali, J (March 2018) Research presentation Who's smelling who? Bi-directional signaling and implications for Multi-trophic chemical ecology.,",International Society for Chemical Ecology, Budapest, Hungary. 2. Ali, J (March 2018) "The 2018 C.V. Riley Lecturer in Entomology", University of Missouri, Columbia, MO. 3. Ali, J. (April 2018). Invited Seminar. Colorado University Boulder, Ecology and Evolutionary Department, Boulder, CO. 4. Ali, J. (June 2018). Invited Seminar. University of Bern, Switzerland. 5. Ali, J. (June 2018). Division of Chemical Ecology, SLU Alnarp, Sweden. 1.5 -hour lecture in ICE-18, Annual short course in Insect Chemical Ecology. 6. Ali, J. (September 2018). Invited Talk. Brazilian Congress of Entomology, Brazil. 7. Ali, J. (Nov 2017). "Who's smelling who? Bi-directional signaling and implications for Multi-trophic chemical ecology.," Entomological Society of America, Denver, CO. Renner 1. October, 2017. Invited seminar: Stevens Institute of Technology, Hoboken, NJ. "Reduce, recycle, reuse: evolution of defense by co-option in arthropods and plants". 2. November, 2017.Invited talk: Entomological Society of America Conference, Denver, CO. "Investigating bombardier beetle defensive chemistry with an explosive mixture of transcriptomics, phylogenetics, and chemical ecology". 3. January, 2018. Invited talk: Plant and Animal Genome Conference, Pacific Biosciences (PacBio) session, San Diego, CA. "Long-Read Sequencing Reveals Complex Genomic Architecture in Independent Carnivorous Plant Lineages". 4. March, 2018. Invited talk: Plant Biology Interdepartmental Graduate Program, University Park, PA (Penn State). "Reduce, recycle, reuse: complex genomic architecture in independent carnivorous plant lineages". 5. July, 2018. Botanical Society of America, Rochester, MN. "Plant carnivory and the evolution of genomic architecture in the Caryophyllales". 6. September, 2018. Invited seminar: University at Buffalo SUNY. "Plant carnivory and the evolution of genomic architecture in the Caryophyllales". What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period Amsalem's lab will continue working on the evolution of ester sterility signal in bees and the brood pheromone in bumblebees. The lab will isolate and identify components of the above pheromones and examine their effect on different aspects related to worker reproduction, colony productivity and social organization. The lab will also investigate the genetic underlying the biosynthesis of Dufour gland esters, and the brain gene expression in response to brood and queen presence in Bombus impatiens. Work will begin on a new collaboration aiming at understanding the synergetic effect of queen behavior and the production of fertility signals on worker reproduction, and whether these queen signals are context dependent. Efforts will be made to identify these co-occurring effects during the transitions of queens between major life cycle events such as mating, colony founding, and during the competition phase, during which the queen is active, yet, no longer able to inhibit worker reproduction. The Tumlinson lab will study the emission of green leaf volatiles (GLV) by plants in response to insect herbivory. The lab will also investigate the mechanisms by which insect herbivore-produced compounds modify GLV production and/or emission by plants. A second project will focus on priming of plant defenses by volatile organic compounds (VOC) from herbivore damaged plants. Target plants will include maize and tobacco. Insect herbivores studied will include Spodoptera exigua, Manduca sexta, Trichoplusia ni and Heliothis virescens. The Tumlinson lab will isolate and identify components of herbivore oral secretions that inhibit and/or modify GLV production and emission. During the next reporting period the Baker lab will continue to try to completely characterize the stereochemical structure of the germacradienol compound we isolated from the sciarid fly fungus gnat, Lycoriella ingenua. The lab will try to complete the isolation and identification of the sex pheromone of the phorid fly mushroom pest, Megaselia halterata by conducting definitive behavioral bioassays of the two synthesized putative pheromone components. The Ali lab will continue during the next reporting period to work on plant toxicity consequences on monarch migration. The lab iwill also further characterize the compounds that are emitted from nematode-infested cadavers to understand the precise blend ratios of molecules required to increase plant resistance. Additional crop species will be tested for enhanced pest resistance after exposure to these compounds. Work will proceed during the next reporting period in employing behavioral assays for insect choice among plants grown following various cover-crop plants and learning more about any differences in different plant species' ability to distinguish plants having high beneficial microbial communities. In greenhouse and field experiments the Ali lab will evaluate how three cover crop species affect crop plant resistance. We will monitor mycorrhizal colonization, corn chemical response, corn resistance to both above- and belowground pests, and their behavior. In addition, the Ali lab will begin working on a new project investigating the impact of spotted lanternfly on the quality of Pennsylvania wines. During the next reporting period, the Renner lab will continue to study the genes responsible for the biosynthesis of ground beetle chemical compounds. Specifically, the lab is interested in (1) whether distantly-related species that produce the same compounds are using the same gene family members, (2) what variation exists at the molecular level, and (3) whether genes involved in biosynthesis have been co-opted from those used in general metabolic processes. The Renner lab will also continue to study the interface between plant nutrient acquisition and defense using carnivorous plants as model organisms. The lab is particularly interested in whether whole genome or tandem duplications are responsible for the prevalence of genes involved in essential nutrient assimilation and deterrence of insect herbivores/pathogenic microorganisms, and to study this, we will continue to use new methods in long-read sequencing to assemble high-quality genomes. In addition, we are interested in whether after a gene duplication event, regulatory divergence in gene expression and function occurs. To determine the degree of cross-talk between the regulation of genes involved in nutrient acquisition and defense, we will apply various nitrogenous substrates and phytohormones to plants in vitro and measure gene expression using methods in comparative transcriptomics.

Impacts
What was accomplished under these goals? We have now demonstrated that caterpillar regurgitant contains two enzyme and one heat-stable small molecule, each of which modifies GLV emission in a different manner. We have isolated and partially purified the small molecule and are conducting experiments to determine its structure. We have now isolated electrophysiologically active compounds from the extracts of female mushroom phorid flies, Megaselia halterata in our ongoing effort to identify the sex pheromone of this pestiferous species of mushrooms. We now have clear evidence that these compounds represent the active sex pheromone blend of this species. We have chemically characterized the chemical structures of two of these compounds that show good electrophysiological activity and that heretofore had never been identified from natural products. In exhaustive field work during 2018 on the invasive species, Lycorma deliculata, the spotted lanternfly (Hemiptera: Fulgoridae), we found that during their flight dispersal behavior the adults launch themselves upwind to traverse ca. 30 - 50 meters in single flight-bouts, which are repeated until a new food source is located. We observed adults launching themselves to land on moving train cars and potentially hitchhiking their way to new locations far from the Pa quarantine zone. We believe our studies will be important in informing government agencies as to the directions and distances that adults can potentially move over the landscape to invade new areas. Pheromones regulating cooperative behavior and social organization in insect societies are one of the supreme puzzles in social evolution. In work on the social bumblebee species Bombus impatiens, we found that first and second instar brood regulate egg laying behavior in adult workers. We showed that the brood effect was general and independent of its sex or relatedness to workers. We further examined how the brood communicates its presence by introducing workers to whole body extracts, body washes or volatiles produced by young larvae using a vacuum air-flow system. However, none of these extracts were able to replicate the full effect of live brood. We also found that young brood and the queen regulate distinct genetic pathways in worker's brain, suggesting that their inhibitory effects are complimentary. In our study of the evolution of Dufour gland produced esters in bees, we examined the transition in the role of esters from purely functional in solitary bees to a communicative role signaling reproductive status in social insects. We identified and quantified the production of esters as function of the social and reproductive condition in Bombus (social) and Osmia (solitary) females. Behavioral and electroantennographic bioassays of female perception and attraction to their own Dufour gland have demonstrated attraction in Bombus but not in Osmia bees. In work on the fire ant, Solenopsis invicta, we identified two missing genes in one of the variants of the social chromosome of workers, and which may play a role in the regulation of the social organization. Fire ants colonies are headed by either a single queen carrying a homozygote variant of the 'social chromosome' (BB) or by multiple queens carrying the heterozygote variant (Bb). Each of the these haplotypes is associated with a particular odor, presumably produced and secreted onto the queen cuticle, allowing the workers to accept or reject queens based on their genotype/odor. We confirmed a deletion of two genes in the genome of heterozygote workers carrying haplotype b, identify them as odorant receptors and showed that the regulation of these genes occur both at the DNA and RNA levels. We have developed a bioassay in workers to discriminate queens based on their genotype and reproductive status, and a non-intrusive method to manipulate the expression level of specific genes in fire ants in order to examine their effect on the social structure. Our research on pathogenesis-related (PR) proteins suggests that during the evolution of carnivory within carnivorous plant lineages, chitinase genes primarily utilized for pathogenesis response by ancestral non-carnivorous plants duplicated and diverged. Through subsequent co-option, the chitinases were then subfunctionalized for pathogenic response versus digestion, substantiated by shifts in selection pressures affecting protein structure and function. Knowledge of the origin and evolution of digestive enzymes has since expanded. OurUtricularia gibba(Lamiales) work has revealed large expansions of defense-related gene families, in addition to genes involved in nutrient acquisition and stress response. Among these are tandem arrays of cysteine protease genes with trap-specific expression that evolved within a protein family already known to be involved in carnivory in other species. The cysteine protease gene family includes papains, which were characterized in papaya and thought to have evolved as part of protection from herbivorous insects. We have since extended study of theCephalotus follicularis(Oxalidales) andDrosera capensis(Caryophyllales) genomes to their own tandemly duplicated gene content, uncovering similar enrichments. On our ground beetle project, to begin to identify the genes responsible for the biosynthesis of over 250 individual compounds produced by members of the ground beetle lineage, we have RNA-sequenced the pygidial gland system for Brachinus elongatulus (bombardier beetle) and Harpalus pensylvanicus (Pa ground beetle). For each of these species, we have identified genes with putative functions in the biosynthesis of quinones and formic acid. Our work on Allium leafminer has thus far successfully focused on: (1)identifying ALM fly-free periods during the season through studies of phenology and delivery of monitoring programs;(2)determining the behavioral response of ALM to variation in host species, host growth stages, and plant volatiles, and quantifying the within-field distribution ofALM infestations;(3)enabling future opportunities for biological control through baseline natural enemy surveys, building on our finding of parasitism in U.S. populations; and(4)improving the use of conventional and organic insecticides to manage ALM through efficacy trials, while minimizing flare-ups of insecticide-resistant onion thrips. With regard to our research on cover crop legacy, we have found that the species of cover crop farmers choose does in fact have legacy effects on the subsequent corn crop's resistance to the European corn borer, and that this legacy is mediated by soil fertility and/or mycorrhizal colonization. We have found in our project concerning entomopathogenic nematodes (EPNs) that EPN-infested insect cadavers emit volatile compounds, and these indirect chemical cues do have plant-synthesized performance-reducing effects on herbivore pests. In this project, we are investigating the influence of EPN chemical cues on plants and insect herbivores, as both cases would have important consequences for protecting plants against herbivore pests. Our group has initiated a pollinator health conservation project funded by NSF linking variation in milkweed defense biochemistry to variation in larval and resulting adult monarch butterfly fitness traits. We are quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology to determine how plant defense affects larval growth and subsequent adult fecundity in reproductively active monarch butterfly cohorts. Using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism, we are examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs and will link these effects to expression of microRNAs controlling traits associated with migratory phenotypes..

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Cohanim AB, Amsalem E, Saad R, Shoemaker D, Privman E. (2018) Evolution of olfactory functions on the fire ant social chromosome (Accepted to Genome Biology and Evolution)
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Amsalem E, Hefetz A. (2018) Pheromone-mediation of female reproduction and reproductive dominance in social species. Journal of Chemical Ecology
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Amsalem E, Grozinger CM. (2018) The importance of holistically evaluating data: a comment on Holman 2018. Behavioral Ecology
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Amsalem E, Grozinger CM. (2017) Evaluating the molecular, physiological and behavioral impacts of CO2 narcosis in bumble bees (Bombus impatiens) Journal of Insect Physiology 101:57-65
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Myrick, A. J. and Baker, T. C. (2018) Increasing signal-to-noise ratio in gas chromatography-electroantennography using a deans switch effluent chopper. J. Chem. Ecol. 44:111-126.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Wei, J., Zhou, Q., Hall, L. Myrick, A., Hoover, K., Shields, K., and Baker, T. C. (2018) Olfactory sensory neurons of the Asian longhorned beetle, Anoplophora glabripennis, specifically responsive to its two aggregation-sex pheromone components. J. Chem. Ecol. 44:637-649.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Rork AM, Renner T (2018) Carabidae semiochemistry: current and future directions. Journal of Chemical Ecology, https://doi.org/10.1007/s10886-018-1011-8.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kannan S, Halter G, Renner T, Waters ER (2018) Patterns of alternative splicing vary between species during heat stress. AoB Plants. doi: 10.1093/aobpla/ply013. Editors Choice.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2018 Citation: Mazin, M., S. S. Andreadis, N. E. Jenkins, K.R. Cloonan, T. C. Baker and E.G. Rajotte (2018) Activity anddistribution of the mushroom phorid fly, Megaselia halterata, in and around commercial mushroom farms. Entomol. Exp. Appl. (In Press)
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2018 Citation: Beck, J.J., Alborn, H.T., Block, A.K.,Christensen, S.A., Hunter, C.T., Rerig, C.C., Seidl-Adams, I., Stuhl, C.J., Torto, B., Tumlinson,. J.H. (2018) Interactions among plants, insects, and microbes: Elucidation of Inter-Organismal Chemical Communications in agricultural ecology. J. Agric. Food Chem.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Castano-Duque, L., Helms, A., Ali, J. G., & Luthe, D. S. (2018). Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore. Journal of chemical ecology, 1-19.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Davidson?Lowe, E., Szendrei, Z., & Ali, J. G. (2018). Asymmetric effects of a leaf?chewing herbivore on aphid population growth. Ecological Entomology.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Malik, R. J., Ali, J. G., & Bever, J. D. (2018). Mycorrhizal composition influences plant anatomical defense and impacts herbivore growth and survival in a life-stage dependent manner. Pedobiologia, 66, 29-35.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Tourtois, J., Ali, J. G., & Grieshop, M. J. (2017). Susceptibility of wounded and intact black soldier fly Hermetia illucens (L.)(Diptera: Stratiomyidae) to entomopathogenic nematodes. Journal of invertebrate pathology, 150, 121-129.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Lan T, Renner T, Ibarra-Laclette E, Farr KM, Chang T-H, Cervantez-Perez SA, Zheng C, Sankoff D, Tang H, Purbojati RW, Putra A, Drautz-Moses DI, Schuster SC, Herrera-Estrella L, Albert VA (2017). Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome. PNAS, www.pnas.org/cgi/doi/10.1073/pnas.1702072114.


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:For bumblebees: scientific community, farmers, beekeepers, general public. For fire ants: Scientific community, USDA/APHIS plant protection and quarantine specialists, general public. For Asian long horned beetle, USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB is threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S.; For mushroom flies (mushroom phorid fly and fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms. For spotted lanternfly: grape growers, tree fruit growers, homeowners in eastern and southeastern Pennsylvania, Pennsylvania hardwood lumber industry. Changes/Problems:In 2016-17 the project added two new P.I.s: Dr. Etya Amsalem and Dr. Tanya Renner. Dr. Renner only just started her appointment in August of 2017, and thus will contribute to the 2017-18 report next year. What opportunities for training and professional development has the project provided?During 2016-17 the project has provided training and professional development for the following personnel: Research Associates/Postdoctoral Researchers: Dr. Irmgard Seidl-Adams Dr. Andrew Myrick Dr. Michael Domingue Dr. Stefanos Andreadis Dr. Kevin Cloonan Dr. Gabriel Villar (new postdoc 11/2016-current) Dr. Anjel Helms ( USDA Fellow Dr. Swayamjit Ray Graduate Students: Arash Maleki: Anne Jones Kevin Cloonan (received PhD in June, 2017) Loyal Hall Bipana P Timilsena Tristan Cofer Jesse Starkey (new student in 9/2017-current) Adam Damon Elizabeth Davidson-Lowe Nursyafiqi Zainuddin Undergraduate students: Ahja Brown (3/2017-current) In addition, 4 undergraduate students have assisted with experiments in the Tumlinson lab and thus gained research experience. Further, through Penn States SROPa student from Virginia State University gained research experience in the Tumlinson lab. Awards and Honors for Graduate Students in 2016-17: Anne Jones Paul R. Heller Memorial Award, Penn State Dept. of Entomology College of Agricultural Sciences Travel Award E. Adams Memorial Grant-In-Aid Kevin Cloonan: Michael Duke Memorial Award, Penn State Dept. of Entomology (2016) Ahja Brown Undergraduate Research Summer award by the College of Agricultural Sciences 2017 Outreach and Service by Graduate Students: Gabriel Villar, Jesse Starkey, Ahja Brown (2017) The Great Insect Fair (volunteers) Department of Entomology, Penn State Jesse Starkey, The annual meeting of the Pennsylvania Beekeeping Association (2017). The role of brood in regulating reproduction in Bombus impatiens workers: A pheromonal or behavioral mechanism? The Great Insect Fair (volunteer) Department of Entomology, Penn State (2017) (Anne Jones, Kevin Cloonan, Loyal Hall) Science Camp (instructor) Machen Retreat and Conference Center, VA (July 2017) (Anne Jones) ESA representative for the Penn State Entomology Graduate Student Association (EGSA) (2016-2017) (Anne Jones, Kevin Cloonan) Anne Jones, Kevin Cloonan: Hosts, Graduate Student Recruitment Weekend: Department of Entomology, Penn State (2017) How have the results been disseminated to communities of interest?Invited Seminars, Presentations at Scholarly/Scientific Meetings Amsalem: August, 2017 Kyoto, Japan. International Society of Chemical Ecology meeting. Presented a poster entitled: Regulation of reproductive division of labor in bumble bees - a solved puzzle or an ongoing mystery? July, 2017. Invited talk in the chemical ecology short course, Penn State University: The regulation of reproductive division of labor in bumble bees colonies April, 2017. Invited seminar, Department of Entomology, University of California Riverside: "The regulation of reproductive division of labor in bumblebee colonies" August 2017, invited talk in the MCIBS retreat, Penn State University: "Social evolution in insect societies" December, 2016, invited talk in the CMIND (Center for Molecular Investigation of Neurological Disorders) seminar, Penn State University: "The whys and hows of social behavior in insects" October 2016, invited talk for undergraduates in the U-RISE program (Undergraduate Research in Science and Engineering), Penn State University: "The whys and hows of social behavior in insects" Baker October 3, 2016. Mushroom Short Course, State College, PA. Delivered a talk entitled: "Zeroing In On the Precise Molecular Configuration of the Sex Pheromone of the Fungus Gnat, Lycoriella ingenua". January 10, 2017. Western Orchard Pest and Disease Management Conference. Portland, Oregon. "History of a Pheromone Mating Disruption Mega-dispenser: MSTRS Pads and Baggies". March 30 - April 7, 2017. Harbin, China. Northeast Forestry University, Harbin. Gave a total of 12 three-hour lectures in an insect chemical ecology course. Gave four two-hour departmental seminars on insect pheromones and neuroethology of insect olfaction. August 27, 2017. Kyoto, Japan. International Society of Chemical Ecology. Invited talk at a symposium on applied uses of semiochemials entitled, "Designing a Mega-dispenser For Sex Pheromone Mating Disruption. September 21, 2017. Villasimius, Sardinia, Italy. European Symposium on Insect Taste and Olfaction. Delivered a talk entitled, "Couple GC/EAD and GC/Behavior assays used to isolate and identify the sex pheromone of the fungus gnat Lycoriella ingenua". Ali " Chemical communication and beneficial insects: Who's smelling who?" Entomology Society of America: Invited Speaker (November 2017) "Is there always asymetry in herbivore performance when they are sharing host plants" (October 2017) St. Olaf College, Biology Department, Northfield, MN " Above- belowground chemical ecology" Wilks University (March 2017) " Multi-trophic interaction and insights into sustainable pest management" UC Davis Entomology, (February 2017) " Multi-trophic interaction and insights into sustainable pest management" Kellogg Biological Research Station, (January 2017) Tumlinson August 25, 2017. Kyoto, Japan. International Society of Chemical Ecology. Invited Plenary Lecture, "Chemical ecology from calling females to talking plants". Baker and Tumlinson hosted the 2017 International Short Course in Insect Chemical Ecology from June 1st to June 15th, 2017. Twelve international guest lecturers from 5 countries took part in presenting lectures in their sub-areas of chemical ecology in addition to 11 PSU chemical ecology faculty who also lectured. The course attracted 32 students from 15 countries: Argentina, Canada, Colombia, England, Ethiopia, Frande, Germany, India, Japan, Kenya, The Netherlands, Nigeria, Sought Africa, Switzerland, and many states from within the U.S. We obtained supporting funds from 5 corporate sponsors who produce products for chemical ecology field application as well as for research. What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period Amsalem's lab will focus in three projects: a continuation of the above two projects in bumblebees and fire ants and a new project studying the evolution of ester sterility signal in bees. The lab will isolate and identify components of the brood pheromone in Bombus impatiens and examine their effect on different aspects related to worker reproduction, colony productivity and social organization. The lab will extend their study on the genetic regulation of worker identification of the queen in fire ants. Efforts will be made to separate the effects of queen genotype and reproductive status on worker behavior and examine the role of selected odorant receptors on worker responses. Work will begin on a new collaboration aiming at understanding the role of Dufour gland produced esters in bees of different social organizations and explore the transition in the role of esters from purely functional role (nest marking, brood cell lining) in solitary insects to a communicative role signaling reproductive status in social insects. The Tumlinson lab will study the emission of green leaf volatiles (GLV) by plants in response to insect herbivory. The lab will also investigate the mechanisms by which insect herbivore-produced compounds modify GLV production and/or emission by plants. A second project will focus on priming of plant defenses by volatile organic compounds (VOC) from herbivore damaged plants. Target plants will include maize and tobacco. Insect herbivores studied will include Spodoptera exigua, Manduca sexta, Trichoplusia ni and Heliothis virescens. The Tumlinson lab will isolate and identify components of herbivore oral secretions that inhibit and/or modify GLV production and emission. During the next reporting period the Baker lab will continue to try to completely characterize the stereochemical structure of the germacradienol compound we isolated from the sciarid fly fungus gnat, Lycoriella ingenua. The lab will initiate the isolation and identification of the sex pheromone of the phorid fly mushroom pest, Megaselia halterata. Work will continue to try to improve the sex pheromone attractant blend of the Asian long horned beetle, Anoplophora glabripennis, and perform new electrophysiological recordings on the maxillary palps and antennae to try to discover active volatile compounds isolated from plant sources. Efforts will be made to uncover behavioral evidence for how males and females of the spotted lanternfly, Lycorma deliculata, find each other for mating, which at present is a complete mystery. A new project funded by APHIS has begun to find new detection and monitoring tools for the newly invasive species, the allium leafminer fly. Work will continue on trying to optimize visual sticky traps and also to try to determine whether or not this species utilizes pheromones for mate-finding. The Ali lab will continue during the next reporting period to work on plant toxicity consequences on monarch migration and await feedback from funding agencies to continue this project. The lab is also further characterizing the compounds that are emitted from nematode-infested cadavers to see the precise molecules required to increase plant resistance, and test additional crop species for enhanced pest resistance after expose to these compounds. Work has now begun on using behavioral assays for insect choice among plants grown following various cover-crop plants to see if there are differences in their ability to distinguish plants with high beneficial microbial communities. An international collaboration has now begun with colleagues in Sweden to evaluate how plant-touch mechanosensation promotes insect resistance. The lab and collaborators has found thus far that contact with the plant alone can change the plant metabolism, making insects perform worse on the plant and also change plant volatiles in a manner that reduces insect preference for said host. In greenhouse and field experiments the Ali lab will evaluate how three cover crop species affect crop plant resistance. We will monitor mycorrhizal colonization, corn chemical response, corn resistance to both above- and belowground pests, and their behavior. This foundational knowledge will advance the prospect that farmers could intentionally select cover crops to affect corn defense against a suite of herbivores.

Impacts
What was accomplished under these goals? In 2016-17 we performed many field experiments to try to understand the movements of a serious pest of mushrooms in the mushroom-growing region of Pennsylvania the mushroom phorid fly, Megaselia halterata. This pest not only plagues mushroom growers, but nearby neighborhoods as well, with some homeowners expressing frustration and anger at these perplexing flies. Trapping experiments showed that the flies do not arise from steamed ("spent") compost piles outside the mushroom houses, nor do they inhabit nearby wood-rows. They are prevalent over lawn areas outside the mushroom houses where we have found clear evidence that that is the location where they mate. We have isolated electrophysiologically active compounds from the extracts of field-captured, flying M. halterata that we have clear evidence represent the active sex pheromone blend of this species. We have made significant progress in chemically characterizing the chemical structures of these compounds. We have made further progress in chemically characterizing the behaviorally active female-emitted sciarid mushroom fly sex pheromone component, a sesquiterpene alcohol (a form of germacradienol), that is highly active in attracting males. We performed electropalpgrams (EPGs) on the labial and maxillary palps of the invasive cerambycid beetle pest of N. American hardwoods, Anoplophora glabripennis, the Asian longhorned beetle. These show that the coeloconic sensilla on the palps are most sensitive to butyraldehde and acetic acid. We found no evidence that the male palps can detect airborne sex-trail pheromone laid down by females providing evidence that the palps must use contact chemoreception to follow females' trails. We performed further field trapping tests in Harbin, China, to try out newly designed "walk-in" traps for monitoring and detection of this species. In exhaustive field work during 2016-17 on the insidious new invasive species, Lycorma deliculata, the spotted lanternfly (Hemiptera: Fulgoridae), we have carefully constructed a phenology of adult activities and behaviors through their adult life. Importantly, we have begun analyzing video records of the in-flight dispersal behaviors of adults to determine how the adults orient before and during flight with respect to wind velocity and direction, as well as responses to visual landmarks. We believe this will be important data to inform government agencies as to the orientation tendencies of adults to move over the landscape in particular directions to invade new areas, so that optimal detection and suppression tactics can be implemented. Pheromones regulating cooperative behavior and social organization in insect societies are one of the supreme puzzles in social evolution. In work on the social species Bombus Impatiens, we found that the queen's brood modulates egg laying behavior in workers, with the highest impact achieved by the presence of young larvae during the first and second instars. A similar effect was achieved when workers were introduced with whole body extracts of young larvae laid by the queen, but not with queen's eggs, pupae or solvent control. We are now working to characterize the potential pheromone and its origin, and to isolate the active compounds in the extraction. In work on the fire ant, Solenopsis invicta, we identified, together with our collaborators, two missing genes in one of the variants of the social chromosome of workers, and which may play a role in the regulation of the social organization. Fire ants colonies are headed by either a single queen carrying a homozygote variant of the 'social chromosome' (BB) or by multiple queens carrying the heterozygote variant (Bb). Each of the these haplotypes is associated with a particular odor, presumably produced and secreted onto the queen cuticle, allowing the workers to accept or reject queens based on their genotype/odor. We confirmed a deletion of two genes in the genome of heterozygote workers carrying haplotype b, identify them as odorant receptors and showed that the regulation of these genes occur both at the DNA and RNA levels, with different expression levels determined by the social structure. We have developed a bioassay in workers to discriminate queens based on their genotype and reproductive status, and we are in the process of developing a non-intrusive method to manipulate the expression level of specific genes in fire ants in order to examine their effect on the social structure.

Publications

  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: August, 2017 Kyoto, Japan. International Society of Chemical Ecology meeting. Presented a poster entitled: Regulation of reproductive division of labor in bumble bees  a solved puzzle or an ongoing mystery?
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2017 Citation: July, 2017. Invited talk in the chemical ecology short course, Penn State University: The regulation of reproductive division of labor in bumble bees colonies
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2017 Citation: April, 2017. Invited seminar, Department of Entomology, University of California Riverside: The regulation of reproductive division of labor in bumblebee colonies
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: August 2017, invited talk in the MCIBS retreat, Penn State University: Social evolution in insect societies
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: December, 2016, invited talk in the CMIND (Center for Molecular Investigation of Neurological Disorders) seminar, Penn State University: The whys and hows of social behavior in insects
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: October 2016, invited talk for undergraduates in the U-RISE program (Undergraduate Research in Science and Engineering), Penn State University: The whys and hows of social behavior in insects
  • Type: Other Status: Accepted Year Published: 2017 Citation: January 10, 2017. Western Orchard Pest and Disease Management Conference. Portland, Oregon. History of a Pheromone Mating Disruption Mega-dispenser:MSTRS Pads and Baggies.
  • Type: Other Status: Accepted Year Published: 2017 Citation: Chemical communication and beneficial insects: Whos smelling who? Entomology Society of America: Invited Speaker (November 2017)
  • Type: Other Status: Accepted Year Published: 2017 Citation: Is there always asymetry in herbivore performance when they are sharing host plants (October 2017) St. Olaf College, Biology Department, Northfield, MN
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Amsalem E, Padilla M, Schreiber P, Altman N, Hefetz A, Grozinger CM. (2017) Do bumble bee (Bombus impatiens) queens signal their reproductive and mating status to their workers? Journal of Chemical Ecology 43(6),563-572
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Padilla M, Amsalem E, Altman N, Hefetz A, Grozinger CM (2016) Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens. Royal Society open science 3 (10), 160576
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Mitchell, R. F., Hall, L. P., Reagel, P. f., McKenna, D. D., Baker, T. C., and Hildebrand, J. G. (2017) Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle. J. Comp. Physiol. A 203:99-199.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Block, A., Vaughan, M. M., Christensen, S. A., Alborn, H. T., and Tumlinson, J. H. (2017) Elevated Carbon Dioxide Reduces Emission of Herbivore Induced Volatiles in Zea mays. Plant, Cell & Environment, doi: 10.1111/pce.12976.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Rigsby, CM, McCartney, NB, Herms, DA, Tumlinson, JH, and Cipollini, D (2017) Variation in the Volatile Profiles of Black and Manchurian Ash in Relation to Emerald Ash Borer Oviposition Preferences. J Chem Ecol. 43:831842.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Ali, J. G. and Agrawal, A. A. (2017), Trade-offs and tritrophic consequences of host shifts in specialized root herbivores. Functional Ecology, 31:153160. doi:10.1111/1365-2435.12698.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hufnagel, M., Schilmiller, A. L., Ali, J. and Szendrei, Z. (2017), Choosy mothers pick challenging plants: maternal preference and larval performance of a specialist herbivore are not linked. Ecological Entomology, 42:3341. doi:10.1111/een.12350.
  • Type: Book Chapters Status: Accepted Year Published: 2016 Citation: Hillier, N. K. and Baker, T. C. (2016) Pheromones of heliothine moths. In J. D. Allison and R. T. Card�, (eds.) Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, pp. 301-333.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Baker, T. C., and Hansson, B. S. (2016) Moth sex pheromone olfaction: flux and flexibility in the coordinated confluences of visual and olfactory pathways. In J. D. Allison and R. T. Card�, (eds.) Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, pp. 139-171.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Cloonan, K.R., Andreadis, S. A., Jenkins, N. E. and Baker, T. C. Attraction, oviposition and larval survival of the fungus gnat, Lycoriella ingenua, on fungal species isolated from adults, larvae and mushroom compost. Mushroom News, Sept. 2017.
  • Type: Other Status: Other Year Published: 2016 Citation: Phorid Fly Fact Sheet, Penn State University Extension. 2016. T.C. Baker, S.A. Andreadis, M. Mazin, and K.R. Cloonan, co-authors.


Progress 07/01/16 to 09/30/16

Outputs
Target Audience:For Asian long horned beetle and buprestid beetle research: USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the ALB and EAB are threatening destruction of hardwood trees; foresters and forest owners in the Northeastern U.S.; For mushroom flies (fungus gnats): mushroom producers in the U.S., homeowners and residents in neighborhoods near mushroom farms. For spotted lanternfly: grape producers, fruit farmers, homeowners in eastern and southeastern Pennsylvania. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?During the initial months of this new project in 2016 (July 1 - Dec. 30) the project has provided training and professional development for the following personnel: Research Associates: Dr. Irmgard Seidl-Adams Dr. Andrew Myrick Dr. Michael Domingue Dr. Stefanos Andreadis Graduate Students: Arash Maleki: Anne Jones: Kevin Cloonan Loyal Hall Bipana P. Timilsena - New student in 2015; nothing to report Tristan Cofer- New student fall 2016 nothing to report Awards and Honors for Graduate Students in 2016: Anne Jones: ICE Student Oral Competition: Insect Chemical Ecology 1st Place (2016) Paul R. Heller Memorial Award, Penn State Dept. of Entomology (2016) College of Agricultural Sciences Travel Award (2016) Kevin Cloonan: ICE Student Oral Competition: Insect Chemical Ecology 2nd Place (2016) Michael Duke Memorial Award, Penn State Dept. of Entomology (2016) Anne Jones - Research Presentation: XXV International Congress of Entomology (ICE), September 2016, Orlando, Florida. Winner, 1st Prize for Oral Presentation. "The Effect of Caterpillar Oral Secretions on Green Leaf Volatiles" Kevin Cloonan - Research Presentation: XXV International Congress of Entomology (ICE), September 2016. Orlando, Florida. Winner, 2nd Prize for Oral Presentation. "Quest to Identify the Attractive Volatile Bouquet of Selected Fungal Species Isolated From the Mushroom Sciarid Fly, Lycoriella ingenua, to gravid female flies." Outreach and Service by Graduate Students: The Great Insect Fair (volunteer) Department of Entomology, Penn State (2016) (Anne Jones, Kevin Cloonan, Loyal Hall) Science Camp (instructor) Machen Retreat and Conference Center, VA (July 2016) (Anne Jones) ESA representative for the Penn State Entomology Graduate Student Association (EGSA) (2016-2017) (Anne Jones, Kevin Cloonan) Anne Jones, Kevin Cloonan: Hosts, Graduate Student Recruitment Weekend: Department of Entomolgy, Penn State (2016) How have the results been disseminated to communities of interest?Tumlinson: Invited Talk: "Potential of Chemical Ecology for Application in IPM" in Symposium "Novel Contributions of Chemical Ecology to Global IPM", International Congress of Entomology, Orlando FL, Sept 26, 2016. Baker. July 1 - 8, 2016. Iguassu Falls, Brazil. International Society of Chemical Ecology meeting. Chaired a symposium on the applied uses of semiochemicals and delivered an invited talk entitled: "A Method for Creating Highly Concentrated Odor Plumes Passively Emanating From Odor Dispensers". October 3, 2016. Mushroom Short Course, State College, PA. Delivered an invited talk entitled: "Zeroing In On the Precise Molecular Configuration of the Sex Pheromone of the Fungus Gnat, Lycoriella ingenua". What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period the Tumlinson lab will study the emission of green leaf volatiles (GLV) by plants in response to insect herbivory. The lab will isolate and identify components of herbivore oral secretions that inhibit and/or modify GLV production and emission. They will also investiage the mechanisms by which insect herbivore-produced compounds modify GLV production and/or emission by plants. A second project will focus on priming of plant defenses by volatile organic compounds (VOC) from herbivore damaged plants. Target plants will include maize and tobacco. Insect herbivores studied will include Spodoptera exigua, Manduca sexta, Trichoplusia ni and Heliothis virescens. During the next reporting period the Baker lab will continue to try to completely characterize the stereochemical structure of the germacradienol compound we isolated from the sciarid fly fungus gnat, Lycoriella ingenua. We will initiate the isolation and identification of the sex pheromone of the phorid fly mushroom pest, Megaselia halterata. We will continue to work to improve the sex pheromone attractant blend of the Asian long horned beetle, Anoplophora glabripennis, and perform new electrophysiological recordings on the maxillary palps and antennae to try to discover active volatile compounds isolated from plant sources. We will try to uncover behavioral evidence for how males and females of the spotted lanternfly, Lycorma deliculata, find each other for mating, which at present is a complete mystery.

Impacts
What was accomplished under these goals? We have identified a small set of fungal species present during mushroom cultivation that are attractive to female sciarid mushroom flies, i.e., the fungus gnat species, Lycoriella ingenua. Some of these were found on the bodies of gravid females and may explain how infestations get started in mushroom houses. Other fungal species having different degrees of attractiveness to females are those commonly found in mushroom compost. We found that some fungal species that were not attractive to females are very strong oviposition stimulants to females, and so we hypothesize that the volatiles from some fungi attract the females to parts of the compost, and other fungi then stimulate the females to lay their eggs there. We found that larvae can develop to adulthood by feeding on the mycelia of only three different fungal species, and for all the other species, the larvae die before making it past the first larval stage. We have also isolated an active female-emitted sciarid mushroom fly sex pheromone component, a sesquiterpene alcohol that is a type of germacradienol, that is highly active in attracting males. This work proves that a compound identified as a sex pheromone in 1980 by a different research group was an erroneous and misleading identification that has hampered research into finding a true and highly active sex pheromone such as the one we have isolated. We are currently attempting to characterize the precise stereochemical structure of this very difficult and first-ever discovered form of germacradienol, and have formed collaborative research efforts with top-notch sesquiterpene chemists from Germany, England, the U. S., and Costa Rica. We made significant progress during since July 2016 in finding ways to improve attractants for the Asian long horned beetle (ALB; Anoplophora glabripennis). We performed a field trapping test in Harbin, China, that helped resolve whether the aldehyde secondary pheromone component can be replaced with two different kinds of anthropogenic analogs. In work on a new invasive species, Lycorma deliculata, the spotted lanternfly (SLF; Hemiptera: Fulgoridae), we collected samples of honeydew emitted by feeding insects, which we observed to be in large all-female aggregations. A detailed phenological observational study of adult males and females was performed to enlighten us about the potential ecological context for any insect semiochemical attraction. A manuscript is being prepared that summarizes this work. We began collecting volatiles from males, females, and male-female combinations on ailanthus tree leaves in the field. The malaria vector Anopheles gambiae is attracted to the American weed, Parthenium hysterophorus that is invasive in large areas of Africa. The mosquito feeds on nectar from the plant and preliminary evidence suggests that chemicals from the plant enhance the malaria parasite in the mosquito. The biosynthesis of herbivore-induced sesquiterpenes (volatile organic compounds that attract natural enemies of the herbivores) is regulated by farnesyl diphosphate synthases in maize. These chemical signals are produced by cells inside the leaf and emitted via the stomata. The opening and closing of stomata regulates release of these semiochemicals.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Domingue, M. J. Lelito, J. P., Myrick A. J., Cs�ka, G., Sz�cs, L., Imrei, Z., and Baker, T. C. (2016) Changes in spectral preferences of a buprestid beetle unfold during stereotypical visual mating approaches. J. Exp. Biol. 219:2837-2843
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Domingue, M. J., Berkebile, J. Steiner, K. Hall, L. P., Cloonan, K. R. Lance, D. and Baker, T. C. (2016) Host condition effects upon Agrilus planipennis (Coleoptera:Buprestidae) captures on decoy-baited branch traps. Eur. J. Entomol. 113:438-445.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Potential of Chemical Ecology for Application in IPM in Symposium Novel Contributions of Chemical Ecology to Global IPM, International Congress of Entomology, Orlando FL, Sept 26, 2016.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: July 1  8, 2016. Iguassu Falls, Brazil. International Society of Chemical Ecology meeting. Chaired a symposium on the applied uses of semiochemicals and delivered a talk entitled: A Method for Creating Highly Concentrated Odor Plumes Passively Emanating From Odor Dispensers.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: October 3, 2016. Mushroom Short Course, State College, PA. Delivered a talk entitled: Zeroing In On the Precise Molecular Configuration of the Sex Pheromone of the Fungus Gnat, Lycoriella ingenua
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Domingue, M. J., Andreadis, S. S., Silk, P. J., Ryall, K. L., and Baker, T. C. (2016) Interaction of visual and chemical cues in promoting attraction of Agrilus planipennis. J. Chem. Ecol. DOI 10.1007/s10886-016-0706-y.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Cloonan, K. R., Andreadis, S. S., and Baker, T. C. (2016) Attraction of female fungus gnats Lycoriella ingenua to mushroom-growing substrates and the green mold Trichoderma aggressivum. Entomol. Exp. Appl. 159:298-304.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Baker, T. C., Zhu, J., and Millar, J. G. (2016) Delivering on the promise of pheromones. J. Chem. Ecol. 42:553-556.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Baker, T. C., Myrick, A. J. and Park, K. C. (2016) Optimizing the point-source emission rates and geometries of pheromone mating disruption mega-dispensers. J. Chem. Ecol. doi:10.1007/s10886-016-0769-9.