Sterile Workers Research Articles

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long‐discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are still debated. We study a simple model of evolutionary dynamics based on haplodiploid genetics. Our model is set in the commonly observed case where workers have lost the ability to lay female (diploid) eggs by mating, but retain the ability to lay male (haploid) eggs. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen‐induced worker sterility. These conditions do not depend on the queen's mating frequency. We find that queen control is always established if it increases colony reproductive efficiency, but can evolve even if it decreases colony efficiency. We further derive the conditions under which queen control is evolutionarily stable against invasion by mutant workers who have recovered the ability to lay male eggs.

Bee larvae fed beebread never become queens

A simple meal is all that is needed to determine the fate of a honeybee larva. It turns out that fragments of genetic material from flowers in their food control the bees' destinies. When female larvae are fed royal jelly, secreted by other bees, they develop into large, fertile queens. But most larvae eat beebread, a mix of pollen and nectar. These larvae develop into small, sterile workers. Xi Chen at Nanjing University in China and colleagues have now found that beebread contains lots of small RNA molecules called microRNAs that regulate the expression of genes.

Honeybee workers with higher reproductive potential live longer lives

Social insects, especially honeybees, have received much attention in comparative gerontology because of their peculiar and flexible ageing patterns that differ across genetically similar individuals. The longevity of honeybee individuals varies and depends on patterns of gene expression during development; females developing into reproductive individuals (queens) live longer than facultatively sterile workers. Here, we show that rebel workers, which develop under queenless conditions after swarming and have high reproductive potential, live approximately 4days longer in hives and approximately 3days longer in cages than individuals that develop in queenright colonies and have lower reproductive potential; this difference in longevity occurs in both free-flying and caged workers. Moreover, we show that both rebel and normal workers live longer when their ovaries contain more ovarioles. Longer-living rebel workers can benefit the colony because they can fill the generation gap that emerges between workers after queen exchange during swarming. Our findings provide novel evidence that the fecundity of workers in a social insect colony impacts their intrinsic longevity.

The Effects of Fat Body Tyramine Level on Gustatory Responsiveness of Honeybees (Apis mellifera) Differ between Behavioral Castes.

Division of labor is a hallmark of social insects. In the honeybee (Apis mellifera) each sterile female worker performs a series of social tasks. The most drastic changes in behavior occur when a nurse bee, who takes care of the brood and the queen in the hive, transitions to foraging behavior. Foragers provision the colony with pollen, nectar or water. Nurse bees and foragers differ in numerous behaviors, including responsiveness to gustatory stimuli. Differences in gustatory responsiveness, in turn, might be involved in regulating division of labor through differential sensory response thresholds. Biogenic amines are important modulators of behavior. Tyramine and octopamine have been shown to increase gustatory responsiveness in honeybees when injected into the thorax, thereby possibly triggering social organization. So far, most of the experiments investigating the role of amines on gustatory responsiveness have focused on the brain. The potential role of the fat body in regulating sensory responsiveness and division of labor has large been neglected. We here investigated the role of the fat body in modulating gustatory responsiveness through tyramine signaling in different social roles of honeybees. We quantified levels of tyramine, tyramine receptor gene expression and the effect of elevating fat body tyramine titers on gustatory responsiveness in both nurse bees and foragers. Our data suggest that elevating the tyramine titer in the fat body pharmacologically increases gustatory responsiveness in foragers, but not in nurse bees. This differential effect of tyramine on gustatory responsiveness correlates with a higher natural gustatory responsiveness of foragers, with a higher tyramine receptor (Amtar1) mRNA expression in fat bodies of foragers and with lower baseline tyramine titers in fat bodies of foragers compared to those of nurse bees. We suggest that differential tyramine signaling in the fat body has an important role in the plasticity of division of labor through changing gustatory responsiveness.

The Impact of Video Feedback on Acquiring Competency in Basic Surgical Skills (Sterile Working) in an Undergraduate Medical Training Program: A Comparative Effectiveness Analysis

The Impact of Video Feedback on Acquiring Competency in Basic Surgical Skills (Sterile Working) in an Undergraduate Medical Training Program: A Comparative Effectiveness Analysis

Group demography affects ant colony performance and individual speed of queen and worker aging

BackgroundThe performance and fitness of social societies mainly depends on the efficiency of interactions between reproductive individuals and helpers. Helpers need to react to the group’s requirements and to adjust their tasks accordingly, while the reproductive individual has to adjust its reproductive rate. Social insects provide a good system to study the interrelations between individual and group characteristics. In general, sterile workers focus on brood care and foraging while the queen lays eggs. Reproductive division of labor is determined by caste and not interchangeable as, e.g., in social mammals or birds. Hence, changing social and environmental conditions require a flexible response by each caste. In the ant Cardiocondyla obscurior, worker task allocation is based on age polyethism, with young workers focusing on brood care and old workers on foraging. Here, we examine how group age demography affects colony performance and fitness in colonies consisting of only old or young workers and a single old or young queen. We hypothesized that both groups will be fully functional, but that the forced task shift affects the individuals’ performance. Moreover, we expected reduced worker longevity in groups with only young workers due to precocious foraging but no effect on queen longevity depending on group composition.ResultsNeither the performance of queens nor that of workers declined strongly with time per se, but offspring number and weight were influenced by queen age and the interaction between queen and worker age. Individual residual life expectancy strongly depended on colony demography instead of physiological age. While worker age affected queen longevity only slightly, exposing old workers to the conditions of colony founding increased their life spans by up to 50% relative to workers that had emerged shortly before colony set-up.ConclusionsThe social environment strongly affected the tempo of aging and senescence in C. obscurior, highlighting the plasticity of life expectancy in social insects. Furthermore, colonies obtained the highest reproductive output when consisting of same-aged queens and workers independent of their physiological age. However, workers appeared to be able to adjust their behavior to the colony’s needs and not to suffer from age-dependent restrictions.

Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, Epiponini)

Eusocial insect reproductive castes (in Hymenoptera, female reproductive queens and sterile workers) differ dramatically in behavior. Castes may differ in the cognitive demands that affect patterns of brain tissue investment. Queens and workers diverge most strongly in the advanced eusocial, or swarm-founding species, where queens do not forage and rarely leave their nests. We asked whether reproductive castes of swarm-founding paper wasps in the tribe Epiponini differed in the relative sizes of their mushroom bodies (MB), a key brain region involved in sensory integration, and in learning and memory. We measured brain-size corrected volumes of the MB dendritic-field neuropils (calyces) and the MB axonal bundles (peducles and lobes) for queens and workers from 16 species of 10 genera of the tribe Epiponini. The subject species spanned much of the epiponine phylogeny, differing in colony size and degree of caste differentiation. Queens had significantly higher relative MB investment than workers, both for the MB in toto and for the MB calyces. The magnitude of queen-worker MB size differences did not covary significantly with body size, but species with larger colonies had stronger caste differences in MB size. A review of caste differences in MB volume across a wide range of social Hymenoptera taxa suggested a positive association of MB investment with social dominance is widespread. Social insect castes (reproducing queens and sterile workers) differ strongly in behavior, particularly in swarm-founding species where queens are largely nest-bound. Caste comparisons are a powerful model for understanding brain/behavior relationships. We measured the relative size of a key insect brain region, the mushroom bodies (MB), in 16 swarm-founding wasp species. MB are involved in sensory integration, and in learning and memory. Queens had relatively larger MB than workers, and the magnitude of the queen-worker differences increased with species average colony size. We suggest the reproductive dominance and social contact of nest-bound queens promotes greater mushroom body investment.

Evolution of queen cuticular hydrocarbons and worker reproduction in stingless bees

Social insect queen pheromones can be interpreted as the queen’s means of sterilizing her workers, or as an honest signal of queen presence that benefits both parties. Co-mapping worker reproductive behaviour and queen cuticular hydrocarbon (CH) composition and quantity on a phylogeny of 21 stingless bee species showed that there are no associations between these traits. Furthermore, three species that have independently evolved facultative worker sterility are unexceptional in their queen CH. Combined, our analysis suggests that the action of stingless bee queen CHs are best interpreted as a signal of queen presence and not as a chemical contraceptive. Co-mapping the incidence of worker reproduction and queen pheromone chemical composition on a phylogeny of stingless bees reveals no association between queen hydrocarbon profiles and worker reproduction.

Proteomic analysis in the Dufour's gland of Africanized Apis mellifera workers (Hymenoptera: Apidae).

The colony of eusocial bee Apis mellifera has a reproductive queen and sterile workers performing tasks such as brood care and foraging. Chemical communication plays a crucial role in the maintenance of sociability in bees with many compounds released by the exocrine glands. The Dufour’s gland is a non-paired gland associated with the sting apparatus with important functions in the communication between members of the colony, releasing volatile chemicals that influence workers roles and tasks. However, the protein content in this gland is not well studied. This study identified differentially expressed proteins in the Dufour’s glands of nurse and forager workers of A. mellifera through 2D-gel electrophoresis and mass spectrometry. A total of 131 spots showed different expression between nurse and forager bees, and 28 proteins were identified. The identified proteins were categorized into different functions groups including protein, carbohydrate, energy and lipid metabolisms, cytoskeleton-associated proteins, detoxification, homeostasis, cell communication, constitutive and allergen. This study provides new insights of the protein content in the Dufour’s gland contributing to a more complete understanding of the biological functions of this gland in honeybees.

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera.

Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.

Novel approach to heritability detection suggests robustness to paternal genotype in a complex morphological trait.

Heritable variation is essential for evolution by natural selection. In Neotropical army ants, the ecological role of a given species is linked intimately to the morphological variation within the sterile worker caste. Furthermore, the army ant Eciton burchellii is highly polyandrous, presenting a unique opportunity to explore heritability of morphological traits among related workers sharing the same colonial environment. In order to exploit the features of this organismal system, we generated a large genetic and morphological dataset and applied our new method that employs geometric morphometrics (GM) to detect the heritability of complex morphological traits. After validating our approach with an existing dataset of known heritability, we simulated our ability to detect heritable variation given our sampled genotypes, demonstrating the method can robustly recover heritable variation of small effect size. Using this method, we tested for genetic caste determination and heritable morphological variation using genetic and morphological data on 216 individuals of E. burchellii. Results reveal this ant lineage (1) has the highest mating frequency known in ants, (2) demonstrates no paternal genetic caste determination, and (3) suggests a lack of heritable morphological variation in this complex trait associated with paternal genotype. We recommend this method for leveraging the increased resolution of GM data to explore and understand heritable morphological variation in nonmodel organisms.

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers.

Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes experienced reduced selection compared with genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also experienced reduced selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory.

Making a queen: an epigenetic analysis of the robustness of the honeybee (Apis mellifera) queen developmental pathway.

Specialized castes are considered a key reason for the evolutionary and ecological success of the social insect lifestyle. The most essential caste distinction is between the fertile queen and the sterile workers. Honeybee (Apis mellifera) workers and queens are not genetically distinct, rather these different phenotypes are the result of epigenetically regulated divergent developmental pathways. This is an important phenomenon in understanding the evolution of social insect societies. Here, we studied the genomic regulation of the worker and queen developmental pathways, and the robustness of the pathways by transplanting eggs or young larvae to queen cells. Queens could be successfully reared from worker larvae transplanted up to 3days age, but queens reared from older worker larvae had decreased queen body size and weight compared with queens from transplanted eggs. Gene expression analysis showed that queens raised from worker larvae differed from queens raised from eggs in the expression of genes involved in the immune system, caste differentiation, body development and longevity. DNA methylation levels were also higher in 3-day-old queen larvae raised from worker larvae compared with that raised from transplanted eggs identifying a possible mechanism stabilizing the two developmental paths. We propose that environmental (nutrition and space) changes induced by the commercial rearing practice result in a suboptimal queen phenotype via epigenetic processes, which may potentially contribute to the evolution of queen-worker dimorphism. This also has potentially contributed to the global increase in honeybee colony failure rates.

Parsing the life-shortening effects of dietary protein: effects of individual amino acids.

High-protein diets shorten lifespan in many organisms. Is it because protein digestion is energetically costly or because the final products (the amino acids) are harmful? To answer this question while circumventing the life-history trade-off between reproduction and longevity, we fed sterile ant workers on diets based on whole proteins or free amino acids. We found that (i) free amino acids shortened lifespan even more than proteins; (ii) the higher the amino acid-to-carbohydrate ratio, the shorter ants lived and the lower their lipid reserves; (iii) for the same amino acid-to-carbohydrate ratio, ants eating free amino acids had more lipid reserves than those eating whole proteins; and (iv) on whole protein diets, ants seem to regulate food intake by prioritizing sugar, while on free amino acid diets, they seem to prioritize amino acids. To test the effect of the amino acid profile, we tested diets containing proportions of each amino acid that matched the ant's exome; surprisingly, longevity was unaffected by this change. We further tested diets with all amino acids under-represented except one, finding that methionine, serine, threonine and phenylalanine are especially harmful. All together, our results show certain amino acids are key elements behind the high-protein diet reduction in lifespan.

The Sins of Man

The Sins of Man Michael Nye (bio) Connectivity was the type of company that called all its locations a “campus,” but when Kane looked around, he saw it for what it was: a former regional airport fifty miles south of his home in St. Louis converted into the main delivery hub for a consumer goods company, the old runways now a massive parking lot surrounded by fences and security checkpoints more appropriate for Homeland Security. Beyond the fence line was a small forest of red maples, their bright branches the first hints of the Ozarks to the south. After exiting his truck, Kane often rested his forearms on its roof and stared into the forest, trying to find the exact spot where, if he walked into the tree line, he could no longer be seen. He wondered if this same thought was what his ex-wife Alice was thinking during those last months of their marriage, when she often stood by the back of the house and stared into the yard: where and how will I disappear completely? He locked the door, trying to mentally leave Alice in the cab of his truck where, under the front seat, he had been driving to and from work with his loaded Beretta. He was an ex-military man, always on time for his shift, never permitting himself to linger too long on the woods. He entered a makeshift lobby, stepping out of the oppressive Missouri heat and into the climate controlled airplane hangar that Connectivity had converted into a clean, sterile work space the length of a football field, and the only sound was the steady and unlocateable hum of electronics. On this end, there were a dozen Eagle’s Nests, each the size and shape of a shipping container. Kane strode to Nest #6, took the three wooden steps to the entry, keyed in, waited for the light over the keypad to change from red to green, and pulled the door open. “What’s the word?” Kane asked. Schroeder, his Eagle’s Nest partner, turned from the monitors. He too was ex-military, with the ruddy complexion of a man who had lived too hard for too long. For ten hours, they shared this windowless box lit almost entirely by the glow of computer and television monitors on all of the four surrounding walls. The floors made of vulcanized rubber hushed their footsteps, and up in the corner opposite the doorway, a Febreze Car Vent Clip worked its magic, filling the room with a chemical “fresh citrus” smell of overripe fruit. Schroeder tilted his chair back. “Ozarks have been quiet today,” Schroeder said. “All week, actually. Control thinks the militia might have another attack planned.” “An organized one?” “That’s the rumor.” “An attack on the planes, or on us?” “Honest, buddy?” Schroder said. “No one knows.” “I thought we took this job to avoid that shit.” “I took this job for the donuts. Got some pretty good donuts here.” This was not hyperbole. Outside, on the hangar floor near the restrooms, there was a long series of banquet tables, covered by thick white tablecloths, stocked solely with donuts and coffee. Sugar and [End Page 80] caffeine: the guys loved it. Kane’s favorite was the S’mores, a donut filled with gooey marshmallow, chocolate icing on top, and sprinkled with finely powdered graham crackers. Best goddamn donut he’s ever had. “Manifest?” Kane asked. “Thirty-six singles,” Schroeder said, passing a clipboard to Kane. “Then a whole bunch in Oklahoma. Here’s to continued good luck.” Kane took his ergonomic chair, slipped headphones over his ears, and adjusted the slim microphone to a place just below his chin, out of his line of vision, keeping the six monitors in front of him visible. His first Drop Mission was in Mississippi. Pretty easy. He checked his monitors, verifying fuel levels, drone weight, merchandise integrity, FAA schedule, weather forecast, and the last maintenance test (logged at 1634 yesterday). Then, clearing all flight security and safety checks, Kane used the flight stick to ease his drone onto the runway. He was eighth in line. From inside his Nest, he couldn’t hear or...

How to make a sterile helper

The sterile worker castes found in the colonies of social insects are often cited as archetypal examples of altruism in nature. The challenge is to explain why losing the ability to mate has evolved as a superior strategy for transmitting genes into future generations. We propose that two conditions are necessary for the evolution of sterility: completely overlapping generations and monogamy. A review of the literature indicates that when these two conditions are met we consistently observe the evolution of sterile helpers. We explain the theory and evidence behind these ideas, and discuss the importance of ecology in predicting whether sterility will evolve using examples from social birds, mammals, and insects. In doing so, we offer an explanation for the extraordinary lifespans of some cooperative species which hint at ways in which we can unlock the secrets of long life.

A novel screen for genes associated with pheromone-induced sterility.

For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile. The evolution of worker reproductive altruism is explained by inclusive fitness theory, but little is known of the genes involved or how they regulate the phenotypic expression of altruism. We previously showed that application of honeybee queen pheromone to virgin fruit flies suppresses fecundity. Here we exploit this finding to identify genes associated with the perception of an ovary-inhibiting social pheromone. Mutational and RNAi approaches in Drosophila reveal that the olfactory co-factor Orco together with receptors Or49b, Or56a and Or98a are potentially involved in the perception of queen pheromone and the suppression of fecundity. One of these, Or98a, is known to mediate female fly mating behaviour, and its predicted ligand is structurally similar to a methyl component of the queen pheromone. Our novel approach to finding genes associated with pheromone-induced sterility implies conserved reproductive regulation between social and pre-social orders, and further helps to identify candidate orthologues from the pheromone-responsive pathway that may regulate honeybee worker sterility.

Social complexity influences brain investment and neural operation costs in ants.

The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)-higher order sensory processing compartments-than the more socially basic Formica subsericea workers. Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina, however, appear to be offset by decreased energetic costs.

Life‐history strategy and behavioral type: risk‐tolerance reflects growth rate and energy allocation in ant colonies

Despite the recent interest in animal personality and behavioral syndromes, there is a paucity of explanations for why distinct behavioral traits should evolve to correlate. We investigate whether such correlations across apparently distinct behavioral traits may be explained by variation in life history strategy among individual ant colonies. Life history theory predicts that the way in which individuals allocate energy towards somatic maintenance or reproduction drives several distinct traits in physiology, morphology, and energy use; it also predicts that an individual's willingness to engage in risky behaviors should depend on reproductive strategy.We use Temnothorax ants, which have been shown to exhibit ‘personalities’ and a syndrome that may reflect risk tolerance at the colony level. We measure colonies' relative investment in growth rate (new workers produced) compared to reproductive effort (males and queens produced). Comparing sterile worker production to reproductive alate production provides a direct measure of how colonies are investing their energy, analogous to investment in growth versus reproduction in a unitary organism. Consistently with this idea, we found that behavioral type of ant colonies was associated with their life history strategy: risk‐tolerant colonies grew faster and invested more in reproduction, whereas risk‐averse colonies had lower growth rate but invested relatively more in workers. This provides evidence that behavioral syndromes can be a consequence of life‐history strategy variation, linking the two fields and supporting the use of an integrative approach.

DNA methylation of Kr-h1 is involved in regulating ovary activation in worker honeybees (Apis mellifera)

A fundamental feature of insect colonies is the presence of a sterile worker caste. In the presence of a queen, worker reproduction is suppressed, leading to degradation of the ovaries. However in the absence of the queen, some young workers activate their ovaries and lay eggs that can result in viable male offspring. The genetic and molecular mechanisms that underlie the regulation of worker sterility are only partially understood, but are of great interest since they are fundamental to the evolution of eusociality. Here, we determine whether DNA methylation of the transcription factor, Kruppel homolog 1 (Kr-h1), is associated with ovary activation in workers of honeybee. Workers were reared under queenless conditions and separated into control and CO2-treated cages (CO2 narcosis is known to suppress ovary activation in queenless workers). Patterns of DNA methylation of Kr-h1 in the ovaries of 7-day-old adult workers showed that non-active ovaries had significantly higher levels of methylation at 4 CpG sites compared to workers with active ovaries. CO2 narcosis inhibited ovary activation, but did not alter methylation levels in non-active ovaries. These findings suggest that methylation of Kr-h1 contributes to the regulation of worker sterility in the honeybee. In addition to the overall finding of differential methylation between ovary-activated and non-activated workers, we found evidence of allele-specific methylation at one site.