Progress 11/19/14 to 09/30/19
Outputs
Target Audience:Scientists from academia, industry, and the general public. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This research represents a collaborative effort between Drs. Xuguo Zhou and Kenneth Haynes at the Department of Entomology, University of Kentucky. Funding from this Hatch Project has provided research opportunities for four Ph.D. students and seven undergraduate students, including one from Department of Entomology, five from the Agricultural and Medical Biotechnology Program at the University of Kentucky, and one from the Transylvania University. How have the results been disseminated to communities of interest?Results from this Hatch Project have been presented at the annual meetings of the Entomology Society of America, international conferences, and several national and international research institutions (invited Departmental Seminars) for the past five years. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
For the past five years, we have comprehensively examined the two overarching hypotheses using an integrated approach. There are two major components in this research, social behavior (e.g., undertaking behavior) and caste differentiation (e.g., worker-presolider-soldier transition and worker-reproductive transition), which, at least partially, maintain the social homeostasis in termites. The following are some of the research highlights: Undertaking, a colony hygiene behavior Eusocial insects frequently face death of colony members as a consequence of living in large groups where the success of the colony is not dependent on the fate of the individual. Whereas death of conspecifics commonly triggers aversion in many group-living species due to risk of pathogens, eusocial insects perform cooperative corpse management. The causes and social context of the death, as well as feeding and nesting ecology of the species, influence the way that corpses are treated. The corpse itself releases cues that dictate the colony's response. As a result, social insects exhibit behavioural responses that promote disease resistance, colony defence, and nutrient recycling. Corpse management represents a unique adaption that enhances colony success, and is another factor that has enabled eusocial insects to be so successful (Sun and Zhou, 2013; Sun et al., 2018; Shi et al., submitted). For the duration of this project, we integrated ethology with chemical ecology and genomics toolsets to comprehensive address the corpse management in the Eastern subterranean termite, Reticulitermes flavipes. Dr. Qian "Karen" Sun, a former student and now an assistant professor at the Louisiana State University, demonstrated that: 1) termite workers cannibalize corpses deceased within 32 hours and bury the ones decomposed for 64 hours; 2) early death cues, 3-octanone and 3-octanol, attract workers to consume the dead; while late death cues, phenol, indole, help workers to locate the corpses, and the accumulation of six fatty acids on corpses induce burial behavior, 3) burial behavior demands more energy inputs, involves more labors and differentially expressed genes, in comparison to nutrient recycling through cannibalism during the undertaking processes, and 4) the interplays between the early and the late death cues allow termites to balance the tradeoffs between nutritional benefits and pathogenic risks of the corpses (Sun et al., 2013; 2017b). Currently, Jizhe Shi, a PhD student, has been focusing on the impacts of different causes of death (both biotic and abiotic factors) and different castes of termite corpses (worker, solider, and nymph) on the undertaking behaviors in R. flavipes. Here, we hypothesize that different causes of death could change the dynamics of the early and late death cues and, consequently, the undertaking behaviors. Results from Jizhe's on-going research support the hypothesis, and we are in the process of drafting manuscripts. Besides undertaking, we also 1) identified and functionally characterized foraging gene orthologs in R. flavipes (Merchant et al., 2019), and 2) documented a cooperative policing behavior in R. flavipes, which regulates reproductive division of labor (Sun et al., submitted). Caste differentiation and "social buffering" in termites The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies, in which one or a few individuals dominate reproduction and suppress worker fertility. The inhibitory effect of the queen has been demonstrated in many species in Hymenoptera, but it remains unclear in termites, where reproductive caste consists of both the queen and the king. In R. flavipes, we showed that reproductive females and males influence worker fertility in a sex-specific pattern (Sun et al., 2017a). They inhibit fertility of workers of the same sex, but stimulate workers of the opposite sex to become replacement reproductives when they lose the mating partner. Soldiers, which are always present in termite colonies, do not affect the process. Our results indicate that sex-specificity is important for regulating reproductive division of labor in termites, and the reproductive stimulation adds to our knowledge of this social regulation. Austin Merchant, a PhD candidate, studied the hormonal regulation of worker-solider caste transition in R. flavipes. Termites possess the most complex caste systems of the eusocial taxa, with totipotent workers capable of differentiating into reproductive and defensive castes outside of the "status quo" molt. Exposure to morphogenetic juvenile hormone (JH) causes workers to transition into soldiers via an intermediate caste called a "presoldier". This transition occurs once an individual's endogenous JH titer reaches a critical threshold, which is unknown and can be influenced by multiple factors. Austin's research demonstrated that the amount of exogenous JH required to trigger caste differentiation was significantly different between the worker-presoldier and presoldier-soldier transitions. Genes putatively involved in the caste differentiation responded differently to excessive vs threshold JH treatments. These combined results suggest that the transition from termite worker to soldier is not a one-step process as is often assumed, but rather that the presoldier stage possesses its own unique physiological and genetic traits that warrant further investigation. In a parallel study, we observed a seasonal variation of soldier numbers within the termite colonies. The endocrinological basis of such variation may rely on differences in 1) the availability of juvenile hormone (JH) within the colony or 2) sensitivity to JH among workers. To address this question, we exposed R. flavipes workers to the same quantity of externally applied JH every other month during a 12-month assay period to examine seasonal variation in the soldier formation. Induction of pre-soldiers, an inter-caste between workers and soldiers, was generally lowest in January and March and rose to plateau in the months after. Empirical evidence presented here supports the hypothesis that differential response to a morphogenetic hormone contributes to seasonal variation in termite soldier numbers. This study reflects the complexity of colony-level regulation of social organization in a eusocial society (Merchant et al., submitted). Li "Lee" Tian, a former student and now an associate professor at the China Agricultural University, has focused primarily on termite soldiers, a highly specialized caste developed exclusively for the colony defense (Tian and Zhou, 2014). Lee's pioneer work on termite soldiers leads to a profound discovery in predator-prey interactions (Tian et al., 2017). Based on a mega-analysis, Preisser and colleagues (2005) suggest that the fitness costs of intimidation (also called "scared to death"), traditionally ignored in predator-prey ecology, and may actually be the dominant facet of trophic interactions. While the impact of predator-induced stress on prey has received considerable attention, there has been far less research into the counter measure of prey. Using R. flavipes as a model system, we document a strong impact of soldier-mediated social buffering on worker responses to cues from both heterospecific and conspecific competitors. The strong impact of soldiers on cue-mediated interactions suggests that the role of this caste may extend beyond the physical defense (Tian et al, 2017). This non-combative effect, which we called "peace of mind", is the counter measurement to alleviate the detrimental impacts of the more dominant non-consumptive effect, or, "scared to death", in the predator-prey interactions.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Merchant, A, DY Song, XW Yang, XR Li, X Zhou. 2019. Candidate foraging gene orthologs in a lower termite, Reticulitermes flavipes. Journal of Experimental Zoology. doi: 10.1002/jez.b.22918. [Epub ahead of print]
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Progress 10/01/17 to 09/30/18
Outputs
Target Audience:Scientists from both academia and industry and the general public Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This research represents a collaborative effort between Drs. Xuguo Zhou and Kenneth Haynes at the Department of Entomology, University of Kentucky. Funding from this project has provided research opportunities for one Ph.D. student, and 5 undergraduate students from the Agricultural and Medical Biotechnology Program at the University of Kentucky. How have the results been disseminated to communities of interest?Results from the above-mentioned research have been presented at the annual meeting of the Entomology Society of America, international conferences, and several research institutions (invited Departmental Seminars). What do you plan to do during the next reporting period to accomplish the goals?For the proposed research, we have accomplished our goals during the funding period. In the next few years, we are hoping to conclude this hatch project by publishing a series of peer-reviewed articles on termite behaviors and caste differentiation. In the meantime, the knowledge gained from this research can be translated to other social insects. Termites are not just "the other" eusocial insects. They belong to the infraorder Isoptera, which consists of about 3,000 species and evolves from cockroaches (Blattodea) 50 million years earlier than eusocial Hymenoptera. Within the Hymenoptera and Isoptera societies, social behaviors are evolved independently; however, the vast majority of these behaviors share convergent traits. Unlike Hymenoptera, which are holometabolous and haplodiploid, termites are hemimetabolous insects in which both sexes are diploid. Thus, the origin and mechanisms governing eusociality in Isoptera. and Hymenoptera are substantially different. That been said, comparisons between independently evolved social behaviors can shed light on the roles of evolutionary conservation versus convergence in the evolution of sociality.
Impacts
What was accomplished under these goals?
OUTPUTS: During this funding period, we approach the social homeostasis in termites from both behavior (undertaking) and caste composition (worker-supplementary reproductive transition) perspectives. Eusocial insects frequently face death of colony members as a consequence of living in large groups where the success of the colony is not dependent on the fate of the individual. Whereas death of conspecifics commonly triggers aversion in many group-living species due to risk of pathogens, eusocial insects perform cooperative corpse management. The causes and social context of the death, as well as feeding and nesting ecology of the species, influence the way that corpses are treated. The corpse itself releases cues that dictate the colony's response. As a result, social insects exhibit behavioural responses that promote disease resistance, colony defence, and nutrient recycling. Corpse management represents a unique adaption that enhances colony success, and is another factor that has enabled eusocial insects to be so successful. In Sun et al., 2018, Philos Trans R Soc Lond B Biol Sci. 5; 373(1754), we comprehensively reviewed the causes of death, the sensory detection of death, and corpse management strategies of social insects. In addition, we provide insights into the evolution of behavioural response to the dead and the ecological relevance of corpse management. Jizhe Shi, a PhD candidate, has continued his study on the impact of corpses generated from different causes of death and various castes on the undertaking behaviors in termites. On the caste differentiation front, we studied the worker-reproductive transition. In social insect colonies, one or a few individuals dominate reproduction and suppress worker fertility. The inhibitory effect of the queen has been demonstrated in many species in Hymenoptera, but it remains unclear in termites, where reproductive caste consists of both the queen and the king. In the eastern subterranean termite, Reticulitermes flavipes, we show that reproductive females and males influence worker fertility in a sex-specific pattern [Sun et al., 2017, Naturwissenschaften, 104(9-10):79]. They inhibit fertility of workers of the same sex, but stimulate workers of the opposite sex to become replacement reproductives when they lose the mating partner. Soldiers, which are always present in termite colonies, do not affect the process. Our results indicate that sex-specificity is important for regulating reproductive division of labor in termites, and the reproductive stimulation adds to our knowledge of this social regulation.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Sun, Q., Haynes, K. F., Hampton, J. D., Zhou, X. (2017). Sex-specific inhibition and stimulation of worker-reproductive transition in a termite, Naturwissenschaften. 2017 Sep 6;104(9-10):79. doi: 10.1007/s00114-017-1501-5.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Sun Q, Haynes KF, Zhou X. (2018). Managing the risks and rewards of death in eusocial insects.
Philos Trans R Soc Lond B Biol Sci. 373(1754). pii: 20170258. doi: 10.1098/rstb.2017.0258.
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Progress 10/01/16 to 09/30/17
Outputs
Target Audience:Scientists from both academia and industry General public Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This research represents a collaborative effort between Drs. Xuguo Zhou and Kenneth Haynes at the Department of Entomology, University of Kentucky. Funding from this project has provided research opportunities for one Ph.D. student, and one undergraduate student researcher at the University of Kentucky. How have the results been disseminated to communities of interest?Results from the above-mentioned research have been presented at the annual forum of Ohio Valley Entomological Association, and several research institutions (invited Departmental Seminars in the US and China). What do you plan to do during the next reporting period to accomplish the goals?For the next funding period, Jizhe will continue his research on the impacts of different cause of death on the undertaking behaviors in termites. Jizhe will test the corpses generated by the contact and bait insecticides, as well as entomopathogenic fungi. Austin will investigate the impacts of overloading solider castes in a termite colony. If time permits, he will study the physiological basis of both "scared to death" and "peace of mind" effects in R. flavipes.
Impacts
What was accomplished under these goals?
PROGRESS: There are two major components in the proposed research, undertaking behavior and caste differentiation. Jizhe Shi, a PhD candidate, studied the impacts of different cause of death on the undertaking behaviors in termites. In the proceeding phase of this research, we found that the eastern subterranean termites, Reticulitermes flavipes, use the early and late death cues to modulate their undertaking behaviors to balance the pathogenic risks and nutritional benefits of corpses (Sun et al., 2017, Functional Ecology, 31:697-706). Different cause of death could change the dynamics of such risk and benefit. Here, we hypothesize that different cause of death could change the dynamics of the early and late death cues and, consequently, the undertaking behaviors. To test this hypothesis, we integrated chemical ecology toolsets with behavioral assays to study the chemical profiles and the corresponding behavioral responses to corpses generated by freezing, heating and desiccation in R. flavipes. Austin Merchant, a first-year PhD candidate, investigated the functions of the soldier caste in termites. Specifically, Austin's project is focusing on the "peace of mind" effects rather than the direct physical defense (aggression) in termite soldiers. Building on our previous knowledge (Tian et al., 2017, Ecology, 98:952-960), we proposed a mechanism to counter the "scared to death", i.e., non-consumptive effects, within the predator-prey interactions. For this first year, Austin studied the hormonal regulation of worker-solider caste transition in R. flavipes. Termites possess the most complex caste systems of the eusocial taxa, with totipotent workers capable of differentiating into reproductive and defensive castes outside of the "status quo" molt. Exposure to morphogenetic juvenile hormone (JH) causes workers to transition into soldiers via an intermediate caste called a "presoldier". This transition occurs once an individual's endogenous JH titer reaches a critical threshold, which is unknown and can be influenced by multiple factors. Here, we hypothesized that termites require different JH thresholds to initiate the worker-presoldier and presoldier-soldier transitions, respectively. To test this hypothesis, R. flavipes workers and presoldiers were exposed, respectively, to paper discs treated with a gradient of JH III. In addition, we compared the temporal gene expression profile in termite heads under the excessive vs threshold JH titers. IMPACT: In social animals, chemical communication plays a critical role in regulating their behaviors. In eusocial termites with limited nutritional resources, corpse represents a valuable food resource but also a risk of pathogenic attack. Jizhe's study highlights termites' capability of distinguishing different cause of death based on the chemical cues and the corresponding behavioral adaptation to navigate their ecological niche. Austin's research demonstrates that the amount of exogenous JH required to trigger caste differentiation was significantly different between the worker-presoldier and presoldier-soldier transitions. Genes putatively involved in the caste differentiation responded differently to excessive vs threshold JH treatments. These combined results suggest that the transition from termite worker to soldier is not a one-step process as is often assumed, but rather that the presoldier stage possesses its own unique physiological and genetic traits that warrant further investigation. Furthermore, depending on the purpose of the research, genetic relevance should be taken into consideration when determining the level of hormone to induce castes in termites or other insect species.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Li Tian, Evan L. Preisser, Kenneth F. Haynes, Xuguo Zhou. 2017. Social buffering in a eusocial invertebrate: termite soldiers reduce the lethal impact of competitor cues on workers. Ecology, 98:952-960.
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Progress 10/01/15 to 09/30/16
Outputs
Target Audience:Scientists from both academia and industry General public Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This research represents a collaborative effort among Drs. Xuguo Zhou and Kenneth Haynes from the Department of Entomology, University of Kentucky, and Qisheng Song at the Division of Plant Sciences, University of Missouri. Funding from this project has provided research opportunities for one Ph.D. student, one undergraduate student researcher, and a temporary laboratory technician at the University of Kentucky. How have the results been disseminated to communities of interest?Results from the proposed research have been presented at regional, national and international conferences (annual meeting of Entomological Society of America, Kentucky Innovation Entrepreneurship Conference, annual forum of Ohio Valley Entomological Association, and International Symposium on Insect Physiology, Biochemistry and Molecular Biology, Guangzhou, China), at research institutions (invited Departmental Seminars in the US and China), and toward the general public. What do you plan to do during the next reporting period to accomplish the goals?Building on this study, we are now investigating factors downstream Met for a comprehensive understanding of the Met signaling involved in the soldier caste differentiation. We hope that future study on JH signaling pathway in caste differentiation will bring new insights into genetic changes mediating evolution of sociality in termites and other social insects.
Impacts
What was accomplished under these goals?
There are two major components in the proposed research, undertaking behavior and caste differentiation. This year we have been focusing on the worker-soldier caste differentiation. In laboratory, presoldier differentiation by workers can be artificially induced by exogenous JHIII, thus providing an ideal model for studying JH signaling pathway mediating caste polyphenism. Here, we hypothesized that Methoprene tolerance (Met), a gene encoding a transcriptional regulator of the basic helix-loop-helix (bHLH)-Per-Arnt-Sim (PAS) domain family and a putative JH receptor, is involved in the JH mediated worker-soldier transition. To test this hypothesis, we first cloned and profiled a Met gene in the Eastern subterranean termite, Reticulitermes flavipes, the most widely distributed termite species in North America. Then, we functionally analyzed the Met under the influence of JH. While the role of JH in caste polyphenism has been well established, molecular mechanisms by which JH is transduced to regulate polyphonic cate differentiation remains unclear. Specifically, key factors mediating the JH action in polyphonic development has not been identified. Although Met has been established as a JH receptor to mediate the anti-metamorphic function, whether it involves in JH-mediated polyphenism remains unknown. This study cloned and functionally characterized Met in R. flavipes using in vivo RNAi. Silencing of RfMet significantly reduced the presoldier formation at the presence of exogenous JHIII. The combined results demonstrated that RfMet is a positive regulator modulating the polyphonic worker-soldier caste differentiation in termites.
Publications
- Type:
Journal Articles
Status:
Accepted
Year Published:
2016
Citation:
Sun, Q., Haynes, K.F. & Zhou, X.G. 2016. Dynamic changes in death cues modulate risks and rewards of corpse management. Functional Ecology. DOI: 10.1111/1365-2435.12754
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Progress 11/19/14 to 09/30/15
Outputs
Target Audience:1) Scientists from both academia and industry 2) General public Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This research represents a collaborative effort between Drs. Xuguo Zhou and Kenneth Haynes from the Department of Entomology, University of Kentucky. Funding from this project has provided research opportunities for two Ph.D. students in Entomology, one undergraduate student in the Agriculture Biotechnology Program, and a temporary laboratory technician (another student graduated from the Agriculture Biotechnology Program) at the University of Kentucky. How have the results been disseminated to communities of interest?Results from the proposed research have been presented at regional, national and international conferences (annual meetings of Entomological Society of America, International Society of Chemical Ecology, Kentucky Innovation Entrepreneurship Conference, and the annual forum of Ohio Valley Entomological Association), at research institutions (invited Departmental Seminars in the US and China), and toward the general public. What do you plan to do during the next reporting period to accomplish the goals?We have obtained a pool of candidate genes to study the undertaking behavior (Objective 1), and we are currently working on the functional analysis of these candidates through dietary RNAi (Objective 2). Later, we will assess the biological consequences when undertaking behavior is compromised (Objective 3). Finally, we would like to understand how termites recognize and respond to nestmate corpses infected with diseases. The entomopathogenic fungus Metarhizium anisopliae will be used in Objective 3 to produce pathogen-infected corpses.
Impacts
What was accomplished under these goals?
There are two major behavioral components in the proposed research, undertaking behavior and caste differentiation. This year we have been focusing on the undertaking, a colony level hygiene behavior. To elucidate the chemical and molecular basis of undertaking behavior, i.e., corpse management, in subterranean termites, we have pursued the following aims: 1) document undertaking response toward nestmates with different postmortem times, 2) investigate the temporal change of postmortem chemicals on corpses, 3) functionally analyze the behavioral effects of early and late death cues, and 4) survey the molecular signatures during undertaking process. Here are some of the research highlights: 1) in the eastern subterranean termite, Reticulitermes flavipes, workers cannibalize corpses deceased within 32 hours and bury the ones decomposed for 64 hours (Aim 1); 2) a temporal profile of death-related chemicals has been established (Aim 2); 3) early death cues, 3-octanone and 3-octanol, attract workers to consume the dead; while late death cues, phenol, indole, help workers to locate the corpses, and the accumulation of six fatty acids on corpses induce burial behavior (Aim 3), and 4), expression profiles during the undertaking processes, including cannibalism and burial of corpses, have been investigated using RNA-Seq, and candidate genes and gene networks involved in corpse management have been identified (Aim 4).
Publications
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