scholarly journals Queen and king recognition in the subterranean termite, Reticulitermes flavipes: Evidence for royal recognition pheromones

2018 ◽  
Author(s):  
Colin Francis Funaro ◽  
Coby Schal ◽  
Edward L Vargo

Royal recognition is a central feature of insect societies, allowing them to maintain the reproductive division of labor and regulate colony demography. Queen recognition has been broadly demonstrated and queen recognition pheromones have been identified in social hymenopterans, but not in termites. Here we describe behaviors that are elicited in workers and soldiers by neotenic queens and kings of the subterranean termite, Reticulitermes flavipes, and demonstrate the chemical basis for the behavior. Workers and soldiers readily perform a lateral or longitudinal shaking behavior upon antennal contact with queens and kings. When royal cuticular chemicals are transferred to live workers or inert glass dummies, they elicit antennation and shaking in a dose-dependent manner. The striking response to reproductives and their cuticular extracts suggests that royal-specific cuticular compounds act as recognition pheromones and that shaking behavior is a clear and measurable queen and king recognition response in this termite species.

2018 ◽  
Vol 115 (15) ◽  
pp. 3888-3893 ◽  
Author(s):  
Colin F. Funaro ◽  
Katalin Böröczky ◽  
Edward L. Vargo ◽  
Coby Schal

Chemical communication is fundamental to success in social insect colonies. Species-, colony-, and caste-specific blends of cuticular hydrocarbons (CHCs) and other chemicals have been well documented as pheromones, mediating important behavioral and physiological aspects of social insects. More specifically, royal pheromones used by queens (and kings in termites) enable workers to recognize and care for these vital individuals and maintain the reproductive division of labor. In termites, however, no royal-recognition pheromones have been identified to date. In the current study, solvent extracts of the subterranean termite Reticulitermes flavipes were analyzed to assess differences in cuticular compounds among castes. We identified a royal-specific hydrocarbon—heneicosane—and several previously unreported and highly royal enriched long-chain alkanes. When applied to glass dummies, heneicosane elicited worker behavioral responses identical to those elicited by live termite queens, including increased vibratory shaking and antennation. Further, the behavioral effects of heneicosane were amplified when presented with nestmate termite workers’ cuticular extracts, underscoring the importance of chemical context in termite royal recognition. Thus, heneicosane is a royal-recognition pheromone that is active in both queens and kings of R. flavipes. The use of heneicosane as a queen and king recognition pheromone by termites suggests that CHCs evolved as royal pheromones ∼150 million years ago, ∼50 million years before their first use as queen-recognition pheromones in social Hymenoptera. We therefore infer that termites and social Hymenoptera convergently evolved the use of these ubiquitous compounds in royal recognition.


2020 ◽  
Author(s):  
Qian Sun ◽  
Jordan D. Hampton ◽  
Kenneth F. Haynes ◽  
Austin Merchant ◽  
Xuguo Zhou

AbstractReproductive conflicts are common in insect societies where helping castes retain reproductive potential. One of the mechanisms regulating the conflicts is policing, a coercive behavior that reduces direct reproduction by other individuals. In eusocial Hymenoptera (ants, bees, and wasps), workers or the queen act aggressively toward fertile workers, or destroy their eggs. In many termite species (order Blattodea), upon the death of primary queen and king, workers or nymphs can differentiate into neotenic reproductives and inherit the breeding position. During this process, competition among neotenics is inevitable, but how this conflict is resolved remains unclear. Here, we report a policing behavior that regulates reproductive division of labor in the eastern subterranean termite, Reticulitermes flavipes. Our results demonstrate that the policing behavior is a cooperative effort performed sequentially by successful neotenics and workers. A neotenic reproductive initiates the attack of the fellow neotenic by biting and displays alarm behavior. Workers are then recruited to cannibalize the injured neotenic. Furthermore, the initiation of policing is age-dependent, with older reproductives attacking younger ones, thereby inheriting the reproductive position. This study provides empirical evidence of policing behavior in termites, which represents a convergent trait shared between eusocial Hymenoptera and Blattodea.


Author(s):  
Qian Sun ◽  
Kenneth F Haynes ◽  
Xuguo Zhou

Abstract In social insects, the reproductive division of labor is often regulated through communication using cuticular hydrocarbons (CHCs) that indicate caste identity and reproductive status. In many termites, workers retain reproductive potential and can differentiate into ergatoid reproductives, and this process is mediated by the presence of reproductives in sex- and age-specific patterns. However, little is known about the variation of CHCs profiles during this transition. In this study, we analyzed the CHC profiles of workers in comparison with ergatoids of different age, sex, and mating status in the eastern subterranean termite, Reticulitermes flavipes (Kollar) (Blattodea: Rhinotermitidae), one of the most widely distributed termite species in the world. Both female and male ergatoids were characterized by the presence of tricosane and a group of long-chain and methyl-branched hydrocarbons (chain length ≥ 33), which were found in significantly lower quantities from workers. In addition, CHC profiles differed between newly differentiated (3–4 d) and old (20–25 d) ergatoids, but no difference in CHC signatures was found between females and males based on identified compounds. Heneicosane, a previously reported royal recognition pheromone in R. flavipes, was not detected in ergatoids examined in this study. The results of caste- and age-dependent variations suggest that CHCs may act as releaser pheromones that mediate caste recognition and age-related interactions between reproductives, but analytical results of identified compounds in this study do not support CHCs as sex-specific primer pheromones that regulate nestmate fertility. Royal pheromones in termites may involve complex hydrocarbon blends and non-hydrocarbon substances that await further investigation.


2021 ◽  
Author(s):  
Yuki Mitaka ◽  
Tadahide Fujita

Abstract Chemical communication underlies the sophisticated colony organization of social insects. In these insects, cuticular hydrocarbons (CHCs) play central roles in nestmate, task, and caste recognition, which contribute to maintenance of the social and reproductive division of labor. Queen-specific CHCs reflect queen fertility status and function as a queen recognition pheromone, triggering aggregation responses around the queens. However, there are only a few studies about the royal recognition mechanism in termites, and particularly, no study has reported about queen-specific CHCs in the species using asexual queen succession (AQS) system, in which the primary queen is replaced by neotenic queens produced parthenogenetically. In this study, we identified the CHC pheromone for neotenic queen recognition in the AQS termite species Reticulitermes speratus. Gas chromatography-mass spectrometry analyses revealed that the relative amount of n-pentacosane was disproportionately greater in the CHC profiles of queens than in the CHC profiles of kings, soldiers, and workers. Furthermore, we investigated the cuticular chemicals of the queen aggregate workers; bioassays demonstrated that n-pentacosane shows a worker arrestant activity in the presence of workers’ cuticular extract. These results suggest that R. speratus workers identify whether each individual is a neotenic queen by recognizing the relatively higher ratio of n-pentacosane in the conspecific CHC background. Moreover, they suggest that termites have evolved queen recognition behavior, independently of social hymenopterans.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Nathan T. Derstine ◽  
Gabriel Villar ◽  
Margarita Orlova ◽  
Abraham Hefetz ◽  
Jocelyn Millar ◽  
...  

AbstractReproductive division of labor in insect societies is regulated through multiple concurrent mechanisms, primarily chemical and behavioral. Here, we examined if the Dufour’s gland secretion in the primitively eusocial bumble bee Bombus impatiens signals information about caste, social condition, and reproductive status. We chemically analyzed Dufour’s gland contents across castes, age groups, social and reproductive conditions, and examined worker behavioral and antennal responses to gland extracts. We found that workers and queens each possess caste-specific compounds in their Dufour’s glands. Queens and gynes differed from workers based on the presence of diterpene compounds which were absent in workers, whereas four esters were exclusive to workers. These esters, as well as the total amounts of hydrocarbons in the gland, provided a separation between castes and also between fertile and sterile workers. Olfactometer bioassays demonstrated attraction of workers to Dufour’s gland extracts that did not represent a reproductive conflict, while electroantennogram recordings showed higher overall antennal sensitivity in queenless workers. Our results demonstrate that compounds in the Dufour’s gland act as caste- and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status.


2020 ◽  
Author(s):  
Nathan T. Derstine ◽  
Gabriel Villar ◽  
Margarita Orlova ◽  
Abraham Hefetz ◽  
Jocelyn Millar ◽  
...  

AbstractReproductive division of labor in insect societies is regulated through multiple concurrent mechanisms, primarily chemical and behavioral. Here, we examined if the Dufour’s gland secretion in the primitively eusocial bumble bee Bombus impatiens signals information about caste, social condition, and reproductive status. We chemically analyzed Dufour’s gland contents across castes, age groups, social and reproductive conditions, and examined worker behavioral and antennal responses to gland extracts.We found that workers and queens each possess caste-specific compounds in their Dufour’s glands. Queens and gynes differed from workers based on the presence of diterpene compounds which were absent in workers, whereas four esters were exclusive to workers. These esters, as well as the total amounts of hydrocarbons in the gland, provided a separation between castes and also between fertile and sterile workers. Olfactometer bioassays demonstrated attraction of workers to Dufour’s gland extracts that did not represent a reproductive conflict, while electroantennogram recordings showed higher overall antennal sensitivity in queenless workers. Our results demonstrate that compounds in the Dufour’s gland act as caste- and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status.


2020 ◽  
Vol 287 (1928) ◽  
pp. 20200780
Author(s):  
Qian Sun ◽  
Jordan D. Hampton ◽  
Austin Merchant ◽  
Kenneth F. Haynes ◽  
Xuguo Zhou

Reproductive conflicts are common in insect societies where helping castes retain reproductive potential. One of the mechanisms regulating these conflicts is policing, a coercive behaviour that reduces direct reproduction by other individuals. In eusocial Hymenoptera (ants, bees and wasps), workers or the queen act aggressively towards fertile workers, or destroy their eggs. In many termite species (order Blattodea), upon the death of the primary queen and king, workers and nymphs can differentiate into neotenic reproductives and inherit the breeding position. During this process, competition among neotenics is inevitable, but how this conflict is resolved remains unclear. Here, we report a policing behaviour that regulates reproductive division of labour in the eastern subterranean termite, Reticulitermes flavipes . Our results demonstrate that the policing behaviour is a cooperative effort performed sequentially by successful neotenics and workers. A neotenic reproductive initiates the attack of the fellow neotenic by biting and displays alarm behaviour. Workers are then recruited to cannibalize the injured neotenic. Furthermore, the initiation of policing is age-dependent, with older reproductives attacking younger ones, thereby inheriting the reproductive position. This study provides empirical evidence of policing behaviour in termites, which represents a convergent trait shared between eusocial Hymenoptera and Blattodea.


Author(s):  
Iris Steitz ◽  
Robert J Paxton ◽  
Stefan Schulz ◽  
Manfred Ayasse

AbstractIn eusocial insects, chemical communication is crucial for mediating many aspects of social activities, especially the regulation of reproduction. Though queen signals are known to decrease ovarian activation of workers in highly eusocial species, little is known about their evolution. In contrast, some primitively eusocial species are thought to control worker reproduction through physical aggression by the queen rather than via pheromones, suggesting the evolutionary establishment of chemical signals with more derived sociality. However, studies supporting this hypothesis are largely missing. Socially polymorphic halictid bees, such as Halictus rubicundus, with social and solitary populations in both Europe and North America, offer excellent opportunities to illuminate the evolution of caste-specific signals. Here we compared the chemical profiles of social and solitary populations from both continents and tested whether (i) population or social level affect chemical dissimilarity and whether (ii) caste-specific patterns reflect a conserved queen signal. Our results demonstrate unique odor profiles of European and North American populations, mainly due to different isomers of n-alkenes and macrocyclic lactones; chemical differences may be indicative of phylogeographic drift in odor profiles. We also found common compounds overproduced in queens compared to workers in both populations, indicating a potential conserved queen signal. However, North American populations have a lower caste-specific chemical dissimilarity than European populations which raises the question if both use different mechanisms of regulating reproductive division of labor. Therefore, our study gives new insights into the evolution of eusocial behavior and the role of chemical communication in the inhibition of reproduction.


Insects ◽  
2021 ◽  
Vol 12 (3) ◽  
pp. 218
Author(s):  
Lucas Carnohan ◽  
Sang-Bin Lee ◽  
Nan-Yao Su

Effective active ingredients in toxicant bait formulations must be non-deterrent to insect feeding behavior at lethal concentrations. This study evaluated feeding deterrence for Coptotermes formosanus Shiraki, C. gestroi (Wasmann), and Reticulitermes flavipes (Kollar) when provided access to cellulose impregnated with various concentrations of the insect molting hormone, 20-hydroxyecdysone (20E). Termites were exposed to 20E concentrations of 200, 500, 1000 and 2000 ppm and to noviflumuron at 5000 ppm in a 24 h choice-test, and the mass of substrate consumption from treated and untreated media pads was compared for each treatment. 20E feeding deterrence was detected at 500, 1000 and 2000 ppm for C. gestroi, and at 2000 ppm for C. formosanus. No significant differences in consumption of treated and untreated substrate was detected at any concentration for R. flavipes. Potential methods for reducing deterrence are discussed.


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