Source: UNIVERSITY OF KENTUCKY submitted to NRP
MANAGING STRESS IN TERMITES: PERSPECTIVES FROM THE BRAIN
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1026549
Grant No.
2021-67034-34975
Cumulative Award Amt.
$180,000.00
Proposal No.
2020-10043
Multistate No.
(N/A)
Project Start Date
Jun 1, 2021
Project End Date
May 31, 2024
Grant Year
2021
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
UNIVERSITY OF KENTUCKY
500 S LIMESTONE 109 KINKEAD HALL
LEXINGTON,KY 40526-0001
Performing Department
Entomology
Non Technical Summary
Termites are major structural pests that cause an estimated $40 billion USD in damage a year worldwide. Damage is caused when termite colonies, which can consist of as many as tens to hundreds of thousands of individuals, infest and consume wooden parts of structures. Because colonies live underground and consume wood from the inside out, infestations generally remain unnoticed until significant damage has already occurred. Therefore, control efforts are primarily focused on preventing new infestations. Synthetic termiticides are the most common and cost-effective form of control and are poured in liquid form around at-risk structures to create a long-lasting barrier that kills any termite passing through it. However, synthetic termiticides are also harmful to beneficial soil invertebrates such as earthworms and springtails. In addition, improper application can lead to groundwater contamination, harming aquatic invertebrates and fish. To develop alternative termite control strategies that are sustainable and environmentally friendly, it is necessary to target specific aspects of termite biology, thereby removing the threat posed to other organisms.One possibility is to take advantage of the unique caste systems present in termites. The majority of a termite colony consists of workers and soldiers: workers are physically weak and responsible for a variety of tasks, including nest construction, foraging, and brood care, while soldiers are physically strong and responsible for defending the colony from intruders. Previous work by our lab has revealed that soldiers may also play a role in managing stress of their nestmates. Workers that are continuously exposed to scent cues from a competitor species will die within one to two days. Death occurs even without physical contact between the worker and any competitors, and combined with the erratic behavior displayed by workers under these conditions implies that it is a result of stress alone. If a soldier is present alongside these workers, however, the workers will not die. Essentially, if a worker knows that a soldier is nearby, it will remain relatively free of stress because it is aware that the soldier will fight off any physical threats that may appear. Soldiers are always present at the periphery of the colony and are therefore always available to provide this "peace of mind" to workers, while themselves appearing to be highly resistant to stress. Disrupting this relationship of stress management between workers and soldiers, or artificially inducing stress in workers could represent feasible routes of termite-specific control.The goal of this project is to investigate the phenomenon of termite "peace of mind" so as to better understand its viability as a target for alternative termite control methods. First, the brains of termite workers and soldier will be directly examined and compared to establish how they differ structurally, with consideration for how these differences may relate to the response of each caste to stress. Next, the stress experienced by termites exposed to competitors will be directly quantified by measuring the levels of specific stress hormones present in the brain at different time points and under different conditions. Finally, the regions of the brain that respond stress will be visualized and compared between workers and soldiers. Together, this project will provide a detailed, comprehensive view of how termite workers and soldiers experience stress alongside a deeper understanding of the role that soldiers play in alleviating stress in workers. This work will establish a rationale while also forming the foundation for future alternative forms of termite control that seek to either disrupt the relationship of stress management between workers and soldiers, or artificially induce stress in workers to induce death of the colony.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
0%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21631101060100%
Knowledge Area
216 - Integrated Pest Management Systems;

Subject Of Investigation
3110 - Insects;

Field Of Science
1060 - Biology (whole systems);
Goals / Objectives
The major goal of this project is to investigate how competitor-induced stress leads to changes in neurochemistry and neurophysiology in different termite castes. The following objectives will be carried out:investigate differences in brain structure between workers and soldiersidentify specific neurochemicals responding to competitor-induced stress in workers and soldiersidentify regions in the brain that respond, chemically, to competitor-induced stress
Project Methods
Objective 1. Categorize differences in brain structure between Reticulitermes flavipes castesReticulitermes flavipes worker and soldier brains will be dissected, then immunostained and fixed as follows: 1 hr in 2% paraformaldehyde (PFA), 3 reps of 15 min in PBS mixed with 10% Triton X-100 (PBST), 1 hr in 5% goat serum, 16-24 hrs in primary antibody nc82, 3 reps of 15 min in PBST, 16-24 hrs in secondary antibody Alexa Fluor goat anti-mouse 546, 3 reps of 15 min in PBST, 4 hrs in 4% PFA, 3 reps of 15 min in PBST. Brains are then placed on a poly-lysine-treated cover slip and submerged in the following for 5 mins each: 30% ethanol, 50% ethanol, 70% ethanol, 95% ethanol, 100% ethanol, 100% ethanol, 100% ethanol, 100% xylene, 100% xylene, 100% xylene. Finally, DPX is used to adhere the cover slip to a microscope slide. After drying for 2 days, slides are imaged using a Leica SP8 DLS confocal microscope. All brains are imaged with identical magnification and speed settings, and confocal image stacks are captured with 1 micron intervals. A minimum of 50 brains will be imaged for each caste.Template brain generation and brain comparison are conducted using the Computational Morphometry Toolkit software package (CMTK; https://www.nitrc.org/projects/cmtk/). CMTK's iterative shape averaging tool will be used to generate worker and soldier template brains using the 10 most symmetrical brains imaged for each respective caste (determined manually). Worker and soldier template brains will then be average using the same tool into a worker-soldier intercaste template brain. All 50 brains from each caste will be compared to the intercaste template using CMTK's registration, reformatx, and warp functions. The outputs of this analysis, in the form of Jacobian maps, will be compared between workers and soldiers using CMTK's ttest function, which computes a pixel-wise unpaired two-tailed t-test between two given groups of images. P-values less than 0.05 will be interpreted as significant.Objective 2. Identify neurochemicals responding to competitor-induced stress in Reticulitermes flavipes workers and soldiersHPLC samples will be collected using the competitor-induced stress assay. A group of 20 R. flavipes termites will be placed in a 3.5-cm diameter Petri dish with narrow slits cut into the wall, which will then be placed inside of a larger 5.5-cm diameter Petri dish containing 40 termites. The inner group will consist of either 20 workers or 19 workers and 1 soldier, while the outer group will consist of 39 workers and 1 soldier from either the same colony as the inner group, or the competitor species Reticulitermes virginicus. Inner group termites will be collected at the following time points: pre-setup, 10 min, 30 min, and 12 hrs post-setup. Collected termites will be snap frozen with liquid nitrogen, decapitated, and stored at -80°C. Samples will be shipped to Dr. Colin Brent at the USDA's Arid Land Agricultural Research Center in Maricopa, Arizona. Dr. Brent will carry out HPLC analysis using standard procedures.The results of HPLC analysis will identify biogenic amines that are elevated in termites exposed to competitor-induced stress. The roles of these amines in the competitor-induced stress response will be validated using RNAi. Genes corresponding to biosynthesis of these amines or coding for receptors of these amines will be selected from the annotated R. flavipes genome possessed by our lab. dsRNA will be synthesized using a commercially available kit and delivered orally. The competitor-induced stress assay will be conducted as described above using either dsRNA-treated termites or untreated control termites in the inner group. Mortality will be recorded at 12-, 24-, 48-, and 72-hours post-setup. Mortality in RNAi-treated groups will be compared across time points and between treated and untreated groups using a two-way ANOVA. P-values less than 0.05 will be interpreted as significant.Objective 3. Identify brain regions responding to competitor-induced stress in Reticulitermes flavipes workers and soldiersThe competitor-induced stress assay will be conducted as described in Objective 2. Inner group termites will be collected at the same time points and their brains will be dissected and prepared for visualization. Immunostaining will follow the process described in Objective 1, with the addition of an antibody targeting one of the biogenic amines identified as responding to competitor-induced stress, which will be used alongside nc82. Images of brains will be captured as described in Objective 1 and template brains will be generated using biogenic amine staining patterns. Comparison of biogenic amine staining patterns between worker and soldier termites will be conducted using CMTK, as described in Objective 1. P-values less than 0.05 will be interpreted as significant.Efforts - Efforts expected are: undergraduate student mentoring, teaching university courses as a guest lecturer and/or teaching assistant, and participation in outreach programs at local schools and community centers.Evaluations - Progress towards project completion will be evaluated at annual graduate committee meetings. The primary mentor, Dr. Xuguo Zhou, will perform additional evaluation in the form of annual reviews required by the University of Kentucky's entomology department for all graduate students.

Progress 06/01/21 to 05/31/24

Outputs
Target Audience:Teaching and laboratory instruction efforts have primarily been aimed at undergraduate and graduate students within the University of Kentucky School of Agriculture. Research results have been disseminated at both national and international conferences attended by entomologists from a wide variety of backgrounds. Changes/Problems:The initial goal of this project was to investigate the neurological effects of competitor cue-induced stress in termites. Previously published research suggested that termite workers exposed to chemical and vibratory cues from a competitor species would show significant mortality, even in the absence of direct physical contact. While seemingly straightforward, my research during the fellowship period indicated a high degree of variation regarding whether termites exposed to competitor cues would show mortality, as well as how severe this mortality would be. Because Objectives 2 and 3 required consistent, reliable mortality in termites exposed to competitor cues, I could not carry them out until being able to produce said consistent, reliable mortality. As a result, a large portion of my work during the fellowship period was focused on investigating the conditions under which mortality occurrsin competitor cue-exposed termite workers. From a more optimistic standpoint, this shift in project focus has allowed me to expand my study of the termite brain to be overall more comprehensive by providing additional time to examine a wider variety of castes in a greater degree of detail than was originally planned. What opportunities for training and professional development has the project provided?Over the course of the fellowship, I was able to attend two conferences: IUSSI (International Union for the Study of Social Insects) 2022 in San Diego and ICE (International Conference of Entomology) 2022 in Helsinki, Finland. In addition, I spent August-October 2022 studying at Dr. Kenji Matsuura's lab at Kyoto University in Kyoto, Japan, where I carried out an investigation of the response of Japanese termite species to competitor cues while also learning termite collection and rearing techniques. How have the results been disseminated to communities of interest?I presented research results at both of the conferences listed above, in addition to giving a research seminar at Kyoto University. Over the fellowship duration, I have also given lectures for two undergraduate courses offered by the University of Kentucky's ABT (Agriculture and Medical Biotechnology) program - ABT 201 (Scientific Method in Biotechnology) and ABT 301 (Technical Writing and Presentations). In ABT 201 lectures I presented my graduate research, while in ABT 301 lectures I gave an overview of the scientific writing process. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? This project primarily focused on two subjects: the structure of the termite brain and the response of termite workers to competitor cues. As listed under Objective 1, my first goal was to characterize differences in brain structure between termite castes in the eastern subterranean termite, Reticulitermes flavipes. Each termite caste differs significantly in both behavioral and sensory capabilities, thus I predicted that such differences would extend to the structure of the brain. Although I initially intended to only examine the brains of workers and soldiers, I was able to incorporate three additional castes - nymphs (immature reproductives), alates (dispersing, nymph-derived reproductives), and ergatoids (worker-derived reproductives). Using an immunostaining protocol adapted from Drosophila and refined over the duration of the fellowship, I was able to produce high quality confocal images of termite brains. Then, using a technique called "deformation based morphometry", I performed pairwise comparisons between castes to identify regions of the brain enlarged in one caste relative to another. Overall, I observed significant differences in brain structure between castes. Workers showed enlargement in the antennal lobes and mushroom bodies which, in other insects, are involved in olfaction and learning, respectively. Reproductives of all types showed enlargement in the optic lobes, which process visual cues, while alates specifically showed expansion in the central body, a region that serves a multifacted role in other insects. Soldiers showed expansion in a region that I could not identify to a distinct brain region, given the lack of information available on the termite brain. Finally, I did not observesexual dimorphism in brain structure within any caste. These results represent the first comprehensive study of caste-biased differences in brain structure in any termite species and provide a foundation for future functional studies examining the role of enlargement in specific regions in certain castes. According to previously published research, termite workers exposed to olfactory and vibratory cues from a competitor species show significant levels of mortality within a few days, even in the absence of direct physical contact with competitors. My initial plan with Objectives 2 and 3 was to investigate how this "competitor cue-induced stress" is reflected in the brain. However, Ifound that the mortality induced through competitor cue exposure is much less consistent than had initially been described, both in terms of the timing and severity of mortality. Thus, it was necessary for me to investigate the specifics of the competitor cue-induced stress phenomenon to see if I could produce consistent mortality that would then allow me to proceed with Objectives 2 and 3. Ultimately, I found that many factors can influence this response. Mortality varies based on the species of termite used, and even within the same species mortality may not be consistent across different colonies. I observed mortality in response to competitor cues in four different termite species -Reticulitermes flavipes,Reticulitermes malletei,Reticulitermes speratus,andReticulitermes miyatakei. The former two are found in the United States, while the latter two are found in Japan. Mortality inR. flavipes,R. speratus, andR. miyatakeiwas approximately 20-40% at 3 days, althoughR. malletei consistentlyexhibited >90% mortality within 2 days. In an attempt to investigate factors that may contribute to variation in competitor cue-induced mortality between colonies of the same species, I compared the responses ofR. flavipes colonies collected from the field to those reared in our lab. In general, lab colonies showed significantly higher mortality than field colonies when exposed to conspecific competitors, indicating that the response of a particular colony to competitor cuesis consistent and can be linked to some as-yet unknown differences in physiology. While I was unfortunately unable to produce consistent mortality until the very end of the fellowship period (experiments withR. malleteiwere conducted in Fall 2023) and was thus unable to carry out Objectives 2 and 3, the work I have carried out provides a much more detailed understanding of the termite response to competitors. The results of this research are described in my dissertation, although I am currently working on adapting the relevant chapter into a publishable article.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2024 Citation: Merchant, A., and Zhou, X. (in press). Caste-biased patterns of brain investment in the subterranean termite Reticulitermes flavipes. iScience.
  • Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Merchant, A., and Zhou, X. (under review). Immunostaining and imaging of termite brains. STAR Protocols.
  • Type: Theses/Dissertations Status: Published Year Published: 2024 Citation: Merchant, A (2024). Polymorphism and plasticity in the termite caste system. Theses and Dissertations--Entomology. 82. https://uknowledge.uky.edu/entomology_etds/82


Progress 06/01/22 to 05/31/23

Outputs
Target Audience: Nothing Reported Changes/Problems:Tests of competitor-induced stress assay in Kyoto and in the United States yielded significant variations in mortality. Source of variation is unclear, as results originally reported by Li et al. suggestconsistent mortality when assay is carried out. Original assay may have possessed design flaws that allowed physical contact between termite groups, as adjusting the design to be more secure through the introduction of a mesh barrieryielded significant drops in mortality. Given the questions and inconsistencies that remain concerning the assay, as well as the amount of time remaining in the project period, examination of the neurochemical basis of competitor-induced stress does not appear feasible. Instead, focus will be placed on the design of the assay, alterations to the assay, and how these factors have influenced mortality. What opportunities for training and professional development has the project provided?Attended International Union for the Study of Social Insects (IUSSI) meeting in San Diego and International Conference of Entomology (ICE) meeting in Helsinki, Finland, both in July. Visited Kyoto University in Japan from August-October to conduct research and gain experience in termite collection/rearing. How have the results been disseminated to communities of interest?Reported results of brain study at IUSSI and ICE meetings. Presented research seminar at Kyoto University. What do you plan to do during the next reporting period to accomplish the goals?Focus will be placed on writing and submitting publications for relevant parts of project and wrapping up remainder of research. May or may not attend another conference, contingent on time.

Impacts
What was accomplished under these goals? Completion of Objective 1, expanded to five termite castes - worker, soldier, ergatoid, nymph, alate. Significant differences in brain structure observed among all castes. Sexual dimorphism not observed witihin castes. Completion of proposed supplementary study at Kyoto University. Initiation of stress response appeared to occur only between two different Reticulitermes species, but even within pairings not all colonies showed sensitivity to competitor. Tests conducted afterward in the United States also showed a high degree of inconsistency in terms of both colonies used and total mortality. Significant alterations to Objectives 2 and 3 are likely necessary and are discussed further in the "Changes/Problems" section.

Publications


    Progress 06/01/21 to 05/31/22

    Outputs
    Target Audience:Lectures were given at two courses offered by the University of Kentucky's ABT (Agricultural and Medical Biotechnology) program - ABT 201 (Scientific Method in Biotechnology)and ABT 301 (Technical Writing and Presentations in Biotechnology). Topic of ABT 201 lecture was termite brain research and life as a graduate student. Topic of ABT 301 lecture was scientific writing. In both cases, target audience reached was undergraduate students in the University of Kentucky's ABT program. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?In terms of professional development, the project has provided opportunities to attend two conferences in July of this year -IUSSI (International Union for the Study of Social Insects) in San Diego and ICE (International Conference of Entomology) in Helsinki, Finland. Through the support provided by this project, arrangements have also been made to visit Kyoto University in Kyoto, Japan from August to October of this year (approximately two and a half months), where I will receive training from Dr. Kenji Matsuura, the world expert on termite ecology. How have the results been disseminated to communities of interest?Current progress will be presented at the IUSSI and ICE conferences in July of this year. What do you plan to do during the next reporting period to accomplish the goals?In terms of research, focus will be placed on the second goal of identifying neurochemicals involved in the response to competitor-induced stress. Research will proceed as initially described. While I am in Kyoto, I will carry out the supplementary study initially described as a complement to the second goal. In terms of training and professional development, I will attend the IUSSI and ICE conferences in July where I will present the current progress of this research, followed by a visit to Kyoto University for approximately two and a half months. In terms of other efforts, I will continue to lecture as I did during this reporting period. Reliant on restrictions related to COVID, I will also participate in outreach activities at local schools.

    Impacts
    What was accomplished under these goals? The major focus for this reporting period was the comparison of worker and soldier brain structure in the eastern subterranean termite, Reticulitermes flavipes. After developing the necessary tools for brain comparison, the brains of worker and soldier termites were dissected and imaged. Comparison of the brains of these two groups revealed large regions that were enlarged in one group relative to the other. Regions enlarged in workers relative tosoldiers include those related to learning and memory, as well as smell. The function of regions enlarged in soldiers relative to workers is currently unclear. Additionally, the brains of sexes within groups were compared; for example, males workers vs. female workers. No sex-based differences ini brain structure were found in either workers or soldiers.

    Publications