Worker Division Of Labor Research Articles

Role of the foraging gene in worker behavioral transition in the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae).

Worker division of labor is predominant in social insects. The foraging (for) gene, which encodes cGMP-dependent protein kinase (PKG), has been implicated in the regulation of behavioral transitions in honeybees, but information regarding its function in other social insects is scarce. We investigated the role of the for (Sifor) gene in the red imported fire ant, Solenopsis invicta, and found that Sifor and PKG exhibited different expression patterns in different castes, body sizes, ages and tissues of fire ants, especially in foragers and nurses. Foragers displayed greater locomotor activity but showed no preference for larval or adult odors, whereas nurses showed lesser locomotor activity but had a strong preference for larval odors. We found that the expression of Sifor was significantly higher in the heads of foragers (compared to nurses). RNA interference-mediated Sifor knockdown in foraging workers induced behavioral transition of foragers toward the nurse phenotype characterized by reduced locomotor activity and a stronger preference for larval odors. By contrast, treating nurses with 8-Br-cGMP, an activator of PKG, resulted in behavioral transition toward the forager phenotype characterized by higher locomotor activity but reduced preference for larval odors. Our results suggest that Sifor plays a critical role in the behavioral transition between foragers and nurses of workers, which may be a promising target for RNAi-based management of worker caste organization in S.invicta. © 2022 Society of Chemical Industry.

Behavioral flexibility in Wasmannia auropunctata (Hymenoptera: Formicidae).

Worker division of labor is a defining trait in social insects. Many species are characterized by having behavioral flexibility where workers perform non-typical tasks for their age depending on the colony’s needs. Worker division of labor and behavioral flexibility were examined in the little fire ant Wasmannia auropunctata (Roger, 1863), for which age-related division of labor has been found. Young workers perform nursing duties which include tending of brood and queens, and colony defense, while older workers forage. When nurses were experimentally removed from the colony, foragers were observed carrying out nursing and colony defense duties, yet when foragers were removed nurses did not forage precociously. We also administered juvenile hormone analog, methoprene, to workers. When methoprene was applied, foragers increased their nursing and defense activities while nurses became mainly idle. The behavioral flexibility of foragers of the little fire ant may be evidence of an expansion of worker’s repertoires as they age; older workers can perform tasks they have already done in their life while young individuals are not capable of performing tasks ahead of time. This may be an important adaptation associated with the success of this ant as an invasive species.

On the Molecular Basis of Division of Labor in Solenopsis invicta (Hymenoptera: Formicidae) Workers: RNA-seq Analysis.

The fire ant Solenopsis invicta Buren is an important invasive pest. Among S. invicta workers behavioral changes depend on age where younger ants are nurses and older ants foragers. To identify potential genes associated with this division of labor, we compared gene expression between foragers and nurses by high-throughput sequencing. In total, we identified 1,618 genes significantly differently expressed between nurses and foragers, of which 542 were upregulated in foragers and 1,076 were upregulated in nurses. Several pathways related to metabolism were significantly enriched, such as lipid storage and fatty acid biosynthesis, which might contribute to the division of labor in S. invicta. Several genes involved in DNA methylation, transcription, and olfactory responses as well as resistance to stress were differentially expressed between nurses and foragers workers. Finally, a comparison between previously published microarray data and our RNA-seq data in S. invicta shows 116 genes overlap, and the GO term myofibril assembly (GO: 0030239) were simultaneously significantly enriched. These results advance knowledge of potentially important genes and molecular pathways associated with worker division of labor in S. invicta. We hope our dataset will provide . candidate target genes to disrupt organization in S. invicta as a control strategy against this invasive pest

Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae).

The evolution of complex societies with obligate reproductive division of labor represents one of the major transitions in evolution. In such societies, functionally sterile individuals (workers) perform many of fitness-relevant behaviors including allomaternal ones, without getting any direct fitness benefits. The question of how such worker division of labor has evolved remains controversial. The reproductive groundplan hypothesis (RGPH) offers a powerful proximate explanation for this evolutionary leap. The RGPH argues that the conserved genetic and endocrinological networks regulating fitness-relevant behavior (e g. foraging and brood care) in their solitary ancestors have become decoupled from actual reproduction in the worker caste and now generate worker behavioral phenotypes. However, the empirical support for this hypothesis remains limited to a handful of species making its general validity uncertain. In this study, we combine data from the literature with targeted sampling of key species and apply phylogenetically controlled comparative analysis to investigate if the key prediction of the RGPH, namely an association between allomaternal behavior and an allomaternal physiological state holds in the largest and most species-rich clade of social insects, the ants. Our findings clearly support the RPGH as a general framework to understand the evolution of the worker caste and shed light on one of the major transition in evolutionary history.

Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.).

Most organisms are constantly faced with environmental changes and stressors. In diverse organisms, there is an anticipatory mechanism during development that can program adult phenotypes. The adult phenotype would be adapted to the predicted environment that occurred during organism maturation. However, whether this anticipatory mechanism is present in eusocial species is questionable because eusocial organisms are largely shielded from exogenous conditions by their stable nest environment. In this study, we tested whether food deprivation during development of the honey bee (Apis mellifera), a eusocial insect model, can shift adult phenotypes to better cope with nutritional stress. After subjecting fifth instar worker larvae to short-term starvation, we measured nutrition-related morphology, starvation resistance, physiology, endocrinology and behavior in the adults. We found that the larval starvation caused adult honey bees to become more resilient toward starvation. Moreover, the adult bees were characterized by reduced ovary size, elevated glycogen stores and juvenile hormone (JH) titers, and decreased sugar sensitivity. These changes, in general, can help adult insects survive and reproduce in food-poor environments. Overall, we found for the first time support for an anticipatory mechanism in a eusocial species, the honey bee. Our results suggest that this mechanism may play a role in honey bee queen-worker differentiation and worker division of labor, both of which are related to the responses to nutritional stress.

Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain.

Nervous and neuroendocrine systems mediate environmental conditions to control a variety of life history traits. Our goal was to provide mechanistic insights as to how neurosecretory signals mediate division of labor in the honey bee (Apis mellifera). Worker division of labor is based on a process of behavioral maturation by individual bees, which involves performing in-hive tasks early in adulthood, then transitioning to foraging for food outside the hive. Social and nutritional cues converge on endocrine factors to regulate behavioral maturation, but whether neurosecretory systems are central to this process is not known. To explore this, we performed transcriptomic profiling of a neurosecretory region of the brain, the pars intercerebralis (PI). We first compared PI transcriptional profiles for bees performing in-hive tasks and bees engaged in foraging. Using these results as a baseline, we then performed manipulative experiments to test whether the PI is responsive to dietary changes and/or changes in juvenile hormone (JH) levels. Results reveal a robust molecular signature of behavioral maturation in the PI, with a subset of gene expression changes consistent with changes elicited by JH treatment. In contrast, dietary changes did not induce transcriptomic changes in the PI consistent with behavioral maturation or JH treatment. Based on these results, we propose a new verbal model of the regulation of division of labor in honey bees in which the relationship between diet and nutritional physiology is attenuated, and in its place is a relationship between social signals and nutritional physiology that is mediated by JH.

Honey bee sociogenomics: a genome-scale perspective on bee social behavior and health

The biology of honey bees involves a host of developmental, behavioral, and physiological components that allow thousands of individual bees to form complex social units. Fueled by a wealth of information from new genomic technologies, a new approach, sociogenomics, uses a focus on the genome to integrate the molecular underpinnings and ultimate explanations of social life. This approach has resulted in a massive influx of data from the honey bee genome and transcriptome, a flurry of research activity, and new insights into honey bee biology. Here, we provide an up-to-date review describing how the honey bee has been successfully studied using this approach, highlighting how the integration of genomic information into honey bee research has provided insights into worker division of labor, communication, caste differences and development, evolution, and honey bee health. We also highlight how genomic studies in other eusocial insect species have provided insights into social evolution via comparative analyses. These data have led to several important new insights about how social behavior is organized on a genomic level, including (1) the fact that gene expression is highly dynamic and responsive to the social environment, (2) that large-scale changes in gene expression can contribute to caste and behavioral differences, (3) that transcriptional networks regulating these behaviors can be related to previously established hormonal mechanisms, and (4) that some genes and pathways retain conserved roles in behavior across contexts and social insect taxa.

Worker division of labor and endocrine physiology are associated in the harvester ant,Pogonomyrmex californicus

In Pogonomyrmex californicus harvester ants, an age-associated division of labor occurs in the worker caste, in which young workers perform in-nest tasks and older workers forage for food. Here, we tested whether this behavioral division is age based or age flexible, and whether it coincides with differential expression of systemic hormones with known roles in behavioral regulation. Whole-body content of juvenile hormone (JH) and ecdysteroids was determined in workers from (1) age-typical colonies, in which a typical age structure is maintained and workers transition across behaviors naturally, and (2) single-cohort colonies, which are entirely composed of same-aged workers, facilitating the establishment of age-independent division of labor. Foragers from both colony types had higher JH and lower ecdysteroid content than workers performing in-nest tasks, suggesting that age is not the sole determinant of worker behavior. This association between hormone content and behavior of P. californicus workers is similar to that previously observed in founding queens of this species. Because these hormones are key regulators of development and reproductive behavior, our data are consistent with the reproductive ground plan hypothesis (RGPH), which posits that the reproductive regulatory mechanisms of solitary ancestors were co-opted to regulate worker behavior.

Cross-species correlation between queen mating numbers and worker ovary sizes suggests kin conflict may influence ovary size evolution in honeybees

During social evolution, the ovary size of reproductively specialized honey bee queens has dramatically increased while their workers have evolved much smaller ovaries. However, worker division of labor and reproductive competition under queenless conditions are influenced by worker ovary size. Little comparative information on ovary size exists in the different honey bee species. Here, we report ovariole numbers of freshly dissected workers from six Apis species from two locations in Southeast Asia. The average number of worker ovarioles differs significantly among species. It is strongly correlated with the average mating number of queens, irrespective of body size. Apis dorsata, in particular, is characterized by numerous matings and very large worker ovaries. The relation between queen mating number and ovary size across the six species suggests that individual selection via reproductive competition plays a role in worker ovary size evolution. This indicates that genetic diversity, generated by multiple mating, may bear a fitness cost at the colony level.

Sensory Response System of Social Behavior Tied to Female Reproductive Traits

BackgroundHoney bees display a complex set of anatomical, physiological, and behavioral traits that correlate with the colony storage of surplus pollen (pollen hoarding). We hypothesize that the association of these traits is a result of pleiotropy in a gene signaling network that was co-opted by natural selection to function in worker division of labor and foraging specialization. By acting on the gene network, selection can change a suite of traits, including stimulus/response relationships that affect individual foraging behavior and alter the colony level trait of pollen hoarding. The ‘pollen-hoarding syndrome’ of honey bees is the best documented syndrome of insect social organization. It can be exemplified as a link between reproductive anatomy (ovary size), physiology (yolk protein level), and foraging behavior in honey bee strains selected for pollen hoarding, a colony level trait. The syndrome gave rise to the forager-Reproductive Ground Plan Hypothesis (RGPH), which proposes that the regulatory control of foraging onset and foraging preference toward nectar or pollen was derived from a reproductive signaling network. This view was recently challenged. To resolve the controversy, we tested the associations between reproductive anatomy, physiology, and stimulus/response relationships of behavior in wild-type honey bees.Methodology/Principal FindingsCentral to the stimulus/response relationships of honey bee foraging behavior and pollen hoarding is the behavioral trait of sensory sensitivity to sucrose (an important sugar in nectar). To test the linkage of reproductive traits and sensory response systems of social behavior, we measured sucrose responsiveness with the proboscis extension response (PER) assay and quantified ovary size and vitellogenin (yolk precursor) gene expression in 6–7-day-old bees by counting ovarioles (ovary filaments) and by using semiquantitative real time RT-PCR. We show that bees with larger ovaries (more ovarioles) are characterized by higher levels of vitellogenin mRNA expression and are more responsive to sucrose solutions, a trait that is central to division of labor and foraging specialization.Conclusions/SignificanceOur results establish that in wild-type honey bees, ovary size and vitellogenin mRNA level covary with the sucrose sensory response system, an important component of foraging behavior. This finding validates links between reproductive physiology and behavioral-trait associations of the pollen-hoarding syndrome of honey bees, and supports the forager-RGPH. Our data address a current evolutionary debate, and represent the first direct demonstration of the links between reproductive anatomy, physiology, and behavioral response systems that are central to the control of complex social behavior in insects.

Signaling Who Does Which Chores

Honey bees divvy up the labor of obtaining food and feeding the young by age: Young adult "nurse" bees feed the larvae, whereas older bees forage. The transition from nurse to forager, which can be accelerated or slowed in response to the needs of the hive, is accompanied by a decrease in nutrient stores. Noting that abundant nutrient stores typically promote synthesis of insulin [or insulin-like peptides (ILPs) in insects] and that insulin/insulin-like growth factor signaling (IIS) has been implicated in the central regulation of feeding-related behavior in Drosophila , Ament et al . investigated the role of IIS in honey-bee behavioral maturation. The abundance of mRNAs encoding the ILP AmIlp1 in brain and the ILP receptors AmInR1 and AmInR2 in abdomen was greater in foragers than in nurses (despite their decreased adiposity). This increase depended on nutritional status; immature bees fed on sugar (which led to forager-like lipid stores) expressed more brain ilp1 and brain and abdominal inR1 than their counterparts fed a more nutrient-rich diet of sugar and pollen. IIS stimulates TOR (target of rapamycin), and administration of the TOR inhibitor rapamycin elicited a seasonally dependent delay in the onset of foraging. Although insulin signaling is typically associated with increased energy metabolism, the expression of genes encoding proteins involved in energy metabolism--notably, five of six in the citrate cycle--was enhanced in the brains of nurse bees compared with foragers, although foragers have higher overall metabolic rates. The authors conclude that, in the honey bee, IIS--which is involved in regulation of metabolism and of feeding behavior in a solitary insect--is associated with regulation of social behavior. S. A. Ament, M. Corona, H. S. Pollock, G. E. Robinson, Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U.S.A. 105 , 4226-4231 (2008). [Abstract] [Full Text]

Genome‐wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera)

A key characteristic of eusocial species is reproductive division of labour. Honey bee colonies typically have a single reproductive queen and thousands of sterile workers. Adult queens differ dramatically from workers in anatomy, physiology, behaviour and lifespan. Young female workers can activate their ovaries and initiate egg laying; these 'reproductive' workers differ from sterile workers in anatomy, physiology, and behaviour. These differences, however, are on a much smaller scale than those observed between the queen and worker castes. Here, we use microarrays to monitor expression patterns of several thousand genes in the brains of same-aged virgin queens, sterile workers, and reproductive workers. We found large differences in expression between queens and both worker groups (~2000 genes), and much smaller differences between sterile and reproductive workers (221 genes). The expression patterns of these 221 genes in reproductive workers are more queen-like, and may represent a core group of genes associated with reproductive physiology. Furthermore, queens and reproductive workers preferentially up-regulate genes associated with the nurse bee behavioural state, which supports the hypothesis of an evolutionary link between worker division of labour and molecular pathways related to reproduction. Finally, several functional groups of genes associated with longevity in other species are significantly up-regulated in queens. Identifying the genes that underlie the differences between queens, sterile workers, and reproductive workers will allow us to begin to characterize the molecular mechanisms underlying the evolution of social behaviour and large-scale remodelling of gene networks associated with polyphenisms.

Reproductive physiology, dominance interactions, and division of labour among bumble bee workers

Abstract. Bumble bee workers (Bombus bifarius, Hymenoptera: Apidae) exhibit aggression toward one another after the colony begins producing female reproductive offspring (the competition phase). Workers in competition phase colonies must continue to perform in‐nest tasks, such as nest thermoregulation, and to forage for food, to rear the reproductives to maturity. Therefore, competition phase workers are faced with potentially conflicting pressures to work for their colonies, or to compete for direct reproduction. The effects of reproductive competition on worker task performance were quantified by measuring relationships of worker body size, reproductive physiology, and aggression with their rates of task performance. If worker division of labour was strongly affected by competition, it was predicted that fecund workers would avoid performing nest maintenance and foraging tasks, focusing instead on reproductive behaviour. Furthermore, it was predicted that fecund workers would dominate their nest mates, and that subordinate workers would perform nonreproductive tasks at higher rates. Worker aggression was associated closely with direct reproductive competition. Both aggression and brood interaction rates were related positively with ooctye development. Furthermore, foraging was associated negatively with ovarian development. However, in‐nest and foraging task performance rates were not associated with social aggression. The results support a partial role for reproductive competition in worker polyethism. Although worker aggression did not directly affect polyethism, reproductively competent workers avoided foraging tasks that would remove them from egg‐laying opportunities. Reproductively competent workers did perform in‐nest tasks, suggesting that these tasks entail little cost in terms of reproductive competition.