scholarly journals Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria

2020 ◽  
Vol 223 (18) ◽  
pp. jeb230599
Author(s):  
Francisco Garcia Bulle Bueno ◽  
Rosalyn Gloag ◽  
Tanya Latty ◽  
Isobel Ronai

ABSTRACTSocial insects are characterised by a reproductive division of labour between queens and workers. However, in the majority of social insect species, the workers are only facultatively sterile. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs. Here, we describe the reproductive anatomy of T. carbonaria workers, virgin queens and mated queens. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers' social environment and diet. The ovaries of T. carbonaria workers that are queenless and fed unrestricted, highly nutritious royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that T. carbonaria might have evolved absolute worker sterility because colonies are unlikely to ever be queenless.

2020 ◽  
Author(s):  
Francisco Garcia Bulle Bueno ◽  
Rosalyn Gloag ◽  
Tanya Latty ◽  
Isobel Ronai

ABSTRACTSocial insect reproduction is characterised by a division of labour. Typically, the queen is the sole reproductive female in the colony and the female workers are non-reproductive. However, in the majority of social insect species the workers are only facultatively sterile and remain capable of laying eggs under some conditions, such as when the queen dies. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs, even if a colony loses its queen. Here we describe the reproductive anatomy of T. carbonaria workers (deactivated ovaries), virgin queens (semi-activated ovaries), and mated queens (activated ovaries). T. carbonaria mated queens have high-volume egg production compared to other female insects as each of their eight ovarioles (filaments of the ovary) produces approximately 40 eggs per day. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers’ social environment (separating them from a queen) and diet (feeding them unrestricted highly nutritious honey bee royal jelly), both conditions which cause ovary activation in bee species where workers are facultatively sterile. The ovaries of T. carbonaria workers that are queenless and fed royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that T. carbonaria might have evolved absolute worker sterility because colonies under natural conditions are unlikely to ever be queenless.


2021 ◽  
Vol 9 ◽  
Author(s):  
Abel Bernadou ◽  
Boris H. Kramer ◽  
Judith Korb

The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.


2010 ◽  
Vol 277 (1701) ◽  
pp. 3793-3800 ◽  
Author(s):  
Luke Holman ◽  
Charlotte G. Jørgensen ◽  
John Nielsen ◽  
Patrizia d'Ettorre

The selective forces that shape and maintain eusocial societies are an enduring puzzle in evolutionary biology. Ordinarily sterile workers can usually reproduce given the right conditions, so the factors regulating reproductive division of labour may provide insight into why eusociality has persisted over evolutionary time. Queen-produced pheromones that affect worker reproduction have been implicated in diverse taxa, including ants, termites, wasps and possibly mole rats, but to date have only been definitively identified in the honeybee. Using the black garden ant Lasius niger , we isolate the first sterility-regulating ant queen pheromone. The pheromone is a cuticular hydrocarbon that comprises the majority of the chemical profile of queens and their eggs, and also affects worker behaviour, by reducing aggression towards objects bearing the pheromone. We further show that the pheromone elicits a strong response in worker antennae and that its production by queens is selectively reduced following an immune challenge. These results suggest that the pheromone has a central role in colony organization and support the hypothesis that worker sterility represents altruistic self-restraint in response to an honest quality signal.


2014 ◽  
Vol 281 (1780) ◽  
pp. 20132502 ◽  
Author(s):  
Harindra E. Amarasinghe ◽  
Crisenthiya I. Clayton ◽  
Eamonn B. Mallon

Insects are at the dawn of an epigenetics era. Numerous social insect species have been found to possess a functioning methylation system, previously not thought to exist in insects. Methylation, an epigenetic tag, may be vital for the sociality and division of labour for which social insects are renowned. In the bumble-bee Bombus terrestris , we found methylation differences between the genomes of queenless reproductive workers and queenless non-reproductive workers. In a follow up experiment, queenless workers whose genomes had experimentally altered methylation were more aggressive and more likely to develop ovaries compared with control queenless workers. This shows methylation is important in this highly plastic reproductive division of labour. Methylation is an epigenetic tag for genomic imprinting (GI). It is intriguing that the main theory to explain the evolution of GI predicts that GI should be important in this worker reproduction behaviour.


2021 ◽  
Author(s):  
Mariana Velasque ◽  
Tan Yongkai ◽  
Andrew W Liu ◽  
Nicholas M Luscombe ◽  
Jai A Denton

Eusocial insects are characterized by the presence of division of labour between reproductive (i.e. workers) and non-reproductive (i.e. queens) individuals. In eusocial insects, such as wasps, ants, honeybees and termites, such reproductive division of labour is mediated by the use of unique pheromones. In eusocial animals, pheromones control two distinct aspects of the division of labour: reproduction and division of tasks amongst workers. It has been suggested that eusociality arose independently on several occasions from pheromone-mediated co-option of pathways regulating the reproductive life cycle of solitary insects. Transcriptomic analysis has supported the co-option of similar pathways in each independently evolved eusocial insect. Using a solitary insect model, we sought to determine if these similar transcriptomic signals resulted from the co-option of similar pathways or varying pathways subject to convergent evolution. We measured the transcriptomic and physiological response of Drosophila melanogaster to pheromones from bumblebees, honey bees, and termites. In each case we observed a strong physiological response - the reduction of ovary size. However, employing conventional differential gene expression analysis and several forms of network analysis, we were unable to detect any conserved pathway or genes acting as a primer for eusociality. This strongly suggests that pheromone-mediated eusociality is the result of convergent evolution. Wherein a physiological response, such as reduced reproductive capacity, acts as the primer for eusociality and is subsequently refined.


2017 ◽  
Vol 284 (1851) ◽  
pp. 20162693 ◽  
Author(s):  
Isobel Ronai ◽  
Michael H. Allsopp ◽  
Ken Tan ◽  
Shihao Dong ◽  
Xiwen Liu ◽  
...  

In the social insects, ovary state (the presence or absence of mature oocytes) and ovary size (the number of ovarioles) are often used as proxies for the reproductive capacity of an individual worker. Ovary size is assumed to be fixed post-eclosion whereas ovary state is demonstrably plastic post-eclosion. Here, we show that in fact ovary size declines as honeybee workers age. This finding is robust across two honeybee species: Apis mellifera and A. cerana . The ovariole loss is likely to be due to the regression of particular ovarioles via programmed cell death. We also provide further support for the observation that honeybee workers with activated ovaries (mature oocytes present) most commonly have five ovarioles rather than a greater or smaller number. This result suggests that workers with more than five ovarioles are unable to physiologically support more than five activated ovarioles and that workers with fewer than five ovarioles are below a threshold necessary for ovary activation. As a worker's ovariole number declines with age, studies on worker ovariole number need to take this plasticity into account.


2008 ◽  
Vol 43 (2-3) ◽  
pp. 161-171 ◽  
Author(s):  
Pierre Martel ◽  
Tibor Kovacs ◽  
Virginie Bérubé

Abstract Pulp and paper mill effluents have been reported to cause changes in reproductive indicators of fish in laboratory and field studies. These changes include reduced egg production and gonad size, and altered hormone levels and expression of secondary sex characteristics. We examined the performance of biotreatment plants for their potential in abating effects of pulp and paper mill effluents on fish reproduction under laboratory conditions. A bleached kraft mill effluent (BKME) treated in an aerated lagoon and a thermomechanical pulp mill effluent (TMPE) treated by aerobic sludge in a sequential batch reactor were selected for study. Mature fathead minnows (Pimephales promelas) were exposed to effluents before and after biotreatment under continuous renewal conditions for 21 days. Egg production was monitored daily, while morphometric parameters (length, weight, gonad size), secondary sexual characteristics, and steroid hormone and vitellogenin levels were measured at the end of the effluent exposure. The effluent from both mills before biotreatment impaired the reproductive capacity of minnows (egg production) at concentrations of 10 and 20% vol/vol, but not at 2% vol/vol. Exposure to biotreated effluents from both mills at concentrations of 2, 10, 20, and 40% vol/vol caused no significant differences in overall reproductive capacity of minnows as compared with controls. These results indicate that biotreatment can significantly improve the quality of a BKME and an effluent from a TMP mill with respect to the reproductive capacity of fish as determined in laboratory tests.


1993 ◽  
Vol 41 (5) ◽  
pp. 441 ◽  
Author(s):  
MF Downes

A two-year study of the social spider Badumna candida at Townsville, Queensland, provided information on colony size and changes over time, maturation synchrony, temperature effects on development, sex ratio, dispersal, colony foundation, fecundity and oviposition. Key findings were that B. candida outbred, had an iteroparous egg-production cycle between March and October, had an even primary sex ratio and achieved maturation synchrony by retarding the development of males, which matured faster than females at constant temperature. There was no overlap of generations, the cohort of young from a nest founded by a solitary female in summer dispersing the following summer as subadults (females) or subadults and adults (males). These findings confirm the status of B. candida as a periodic-social spider (an annual outbreeder), in contrast to the few known permanent-social spider species whose generations overlap. Cannibalism, normally rare in social spiders, rose to 48% when spiders were reared at a high temperature. This may be evidence that volatile recognition pheromones suppress predatory instincts in social spiders.


2016 ◽  
Vol 12 (11) ◽  
pp. 20160542 ◽  
Author(s):  
Victoria Norman ◽  
Hugo Darras ◽  
Christopher Tranter ◽  
Serge Aron ◽  
William O. H. Hughes

The reproductive division of labour between queen and worker castes in social insects is a defining characteristic of eusociality and a classic example of phenotypic plasticity. Whether social insect larvae develop into queens or workers has long been thought to be determined by environmental cues, i.e. larvae are developmentally totipotent. Contrary to this paradigm, several recent studies have revealed that caste is determined by genotype in some ant species, but whether this is restricted to just a few exceptional species is still unclear. Here, we show that the Mediterranean harvester ant Messor barbarus possesses an unusual reproductive system, in which the female castes are genetically determined. Using both nuclear and mitochondrial data, we show that Iberian populations have two distinct, cryptic lineages. Workers are always inter-lineage hybrids whereas queens are always produced from pure-lineage matings. The results suggest that genetic caste determination may be more widespread in ants than previously thought, and that further investigation in other species is needed to understand the frequency and evolution of this remarkable reproductive system.


2017 ◽  
Vol 69 (6) ◽  
pp. 660-673 ◽  
Author(s):  
Anjan Pal ◽  
Alton Y.K. Chua ◽  
Dion Hoe-Lian Goh

Purpose In the wake of a rumor outbreak, individuals exchange three types of messages: rumor messages, counter-rumor messages, and uncertainty-expressing messages. However, the properties of the three types of messages are relatively unknown particularly in the social media context. Hence, the purpose of this paper is to examine these three types of messages posted on social media in the wake of a rumor outbreak. Design/methodology/approach Data included tweets posted after the outbreak of a rumor that wrongly accused the fast food chain Kentucky Fried Chicken (KFC) for selling rats instead of chicken. Using a deductive approach, codes were derived via content analysis on the tweets. Volume and exposure of tweets were also examined. Findings Counter-rumor tweets (52 percent) outnumbered rumors tweets (32 percent) and uncertainty-expressing tweets (16 percent). Emotions and personal involvement were abundant in rumor tweets. Expressions of credence and references to URLs were high in counter-rumor tweets. Social ties were found widely in uncertainty-expressing tweets. The high volume and exposure of counter-rumor tweets compared with those of either rumor tweets or uncertainty-expressing tweets highlight the potential of counter-rumors to mitigate rumors. Originality/value This research ventures into a relatively unexplored territory by concurrently examining rumor messages, counter-rumor messages and uncertainty-expressing messages in the wake of a rumor outbreak. It reveals that counter-rumor messages have the potential to mitigate rumors on social media.


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