Robert E. Page

The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein.

Haplodiploid organisms comprise about 20% of animals. Males develop from unfertilized eggs while females are derived from fertilized eggs. The underlying mechanisms of sex determination, however, appear to be diverse and are poorly understood. We have dissected the complementary sex determiner (csd) locus in the honeybee to understand its molecular basis. In this species, csd acts as the primary sex-determining signal with several alleles segregating in populations. Males are hemizygous and females are heterozygous at this locus; nonreproducing diploid males occur when the locus is homozygous. We have characterized csd by positional cloning and repression analysis. csd alleles are highly variable and no transcription differences were found between sexes. These results establish csd as a primary signal that governs sexual development by its allelic composition. Structural similarity of csd with tra genes of Dipteran insects suggests some functional relation of what would otherwise appear to be unrelated sex-determination mechanisms.

The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.

The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.).

Abstract Honey bee foragers were tested for their proboscis extension response (PER) to water and varying solutions of sucrose. Returning pollen and nectar foragers were collected at the entrance of a colony and were assayed in the laboratory. Pollen foragers had a significantly higher probability of responding to water and to lower concentrations of sucrose. Bees derived from artificially selected high- and low-pollen-hoarding strains were also tested using the proboscis extension assay. Returning foragers were captured and tested for PERs to 30% sucrose. Results demonstrated a genotypic effect on PERs of returning foragers. The PERs of departing high- and low-strain foragers were consistent with those of returning foragers. The PERs were related to nectar and water reward perception of foragers. High strain bees were more likely to return with loads of water and lower concentrations of sucrose than foragers from the low pollen strain. Low-strain bees were more likely to return empty. We identified a previously mapped genomic region that contains a variable quantitative trait locus that appears to influence sucrose response thresholds. These studies demonstrate a gene-brain-behavior pathway that can be altered as a consequence of colony-level selection for quantities of stored food.

On being the right size: male contributions and multiple mating in social Hymenoptera

SummaryA number of hypotheses for the occurrence of multiple mating by queens of social Hymenoptera are reviewed in the light of Coles (1983) observation that polyandrous species tend to have larger colonies than single-mating ones. Most of these hypotheses cannot be definitively excluded, but only three of them appear sufficiently general, plausible and predictive to be useful guides to further research. These, and their predictions, are: (1) Caste-determination has a genetic basis and hence polyandry allows fuller expression of the potential caste system in each colony. Species with more complex caste differentiation should be more often polyandrous than species with simpler caste systems. (2) Polyandry maximises the production of divergent worker genotypes and hence the range of environmental conditions that a colony can tolerate. Broader-niched species should be more often polyandrous than species with narrower niches. (3) The reduction of the variance of diploid male production, under the heterozygosity sex-determination model, favors polyandry when sexuals are produced late during colony growth. Queens in species reproducing during the exponential phase of colony growth should tend to mate once, but queens should tend to be polyandrous in species with reproduction occurring further along the colony growth curve. Williamss (1975) observation that the level of genetic variation in a brood approaches a maximum very quickly with increasing polyandry is quantified for females; the initial increase is much greater for male-haploid than for male-diploid species.

Hormonal and Genetic Control of Behavioral Integration in Honey Bee Colonies

The ability of insect colonies to adjust the division of labor among workers in response to changing environmental and colony conditions, coupled with research showing genetic effects on the division of labor in honey bee colonies, led to an investigation of the role of genetics and the environment in the integration of worker behavior. Measurements of juvenile hormone(JH) titers and allozyme analyses of worker honey bees suggest that two processes are involved in colony-level regulation of division of labor: (i) plasticity in age-dependent behavior is a consequence of modulation of JH titers by extrinsic factors, and (ii) stimuli that can affect JH titers and age-dependent behavior do elicit variable responses among genetically distinct subpopulations of workers within a colony. These results provide a new perspective on the developmental plasticity of insect colonies and support the emerging view that colony genetic structure affects behavioral organization.

Aging and development in social insects with emphasis on the honey bee, Apis mellifera L.

Honey bee colonies typically consist of about 20-40 thousand workers, zero to few thousand males (drones), depending on the time of year, and a single queen, the mother of the colony. Workers typically live 3-6 weeks during the spring and summer and can live about 4months during the winter. Queens are longer lived. Anecdotes of queens living 2-3years are not unusual, though they normally live less than a year in commercial hives. Little is known about the life span of drones. Queens develop from fertilized eggs that are not different from the eggs that develop into workers. Queens are, however, twice as large, have specialized anatomy, live much longer, and develop faster from egg to adult. All of these differences are derived from differences in larval rearing environment, primarily nutrition. The developmental trajectory of a female larva from worker into a queen can be determined as late as the third day of larval development, after this time the developmental pathway is fixed for a worker phenotype. The total time of larval development is only 5-6 days, therefore, just 2-3 days of differential feeding can lead to profound differences in development, and longevity. Workers undergo age development after they become adults. Workers usually initiate foraging behavior when they are 2-3 weeks old. The age at which a worker initiates foraging is a strong determinant of her length of life. This is presumed to be a result of the hazards of foraging, but natural senescence also occurs. Some bees remain in the nest and are never observed to forage, thereby outliving their forager sisters. Corresponding to this behavioral development are changes in the sizes of glands and the production of glandular products, increases in biogenic amine titers within the brain, an increase in the volume of specific regions of the brain, and changes in the neural system that affect perception of stimuli, and learning and memory. These age-related changes in behavior are regulated by intrinsic and extrinsic factors. Genetic variation has been demonstrated for many of these life history and behavioral traits. Selection and genome mapping studies have demonstrated relationships between the neural system, behavior, and life history traits.

Complex social behaviour derived from maternal reproductive traits.

A fundamental goal of sociobiology is to explain how complex social behaviour evolves, especially in social insects, the exemplars of social living. Although still the subject of much controversy, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes to result in sib-care, the hallmark of highly evolved social life in insects. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.

Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae)

SummaryThe currently accepted model for division of labor in honey bees, Apis mellifera, explains variation in the frequency at which workers perform specific tasks as the result of differences in age and environment. Although well documented, the model is incomplete because it fails to take genotypic variability among workers into account. We show that workers from two genetically distinct strains of honey bees differed in the age at which they began foraging and in the relative frequency at which they foraged for pollen. Workers from the two strains also exhibited significant spatial heterogeneity within the nest, suggesting that they differed in the frequency at which they performed within-nest tasks as well. A heuristic model of division of labor that incorporates genotypic effects is presented.

The genetics of division of labour in honey bee colonies

Publisher Summary This chapter describes genetic characteristics that are unique to the hymenoptera, including honeybees, and presents how these characteristics, when combined with the mating behavior of queens, affect the genetic “structure” and populations of honeybee colonies. The chapter presents results that demonstrate the fundamental elements of division of labor among workers and suggests how colony-level natural selection adapts populations of colonies to their environment via changes in the behavior of individual, effectively sterile workers. It also presents theoretical models that suggest that some properties of division of labor, such as the occurrence of labor specialists and the ability to reallocate labor in the face of a changing environment, are a consequence of self-organization that may be intrinsic to many types of complex systems, including insect colonies.

The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.).

Abstract Bees derived from artificially selected high- and low-pollen-hoarding strains were tested for their proboscis extension reflex response to water and varying sucrose concentrations. High-strain bees had a lower response threshold to sucrose than low-strain bees among pre-foragers, foragers, queens and drones. Pre-foraging low-strain workers showed ontogenetic changes in their response threshold to sucrose which was inversely related to age. High-strain foragers were more likely to return with loads of water compared to low-strain foragers. Whereas low-strain foragers were more likely to return with loads of nectar. Low-strain nectar foragers collected nectar with significantly higher sucrose concentrations than did the high-strain nectar foragers. Alternatively, low-strain foragers were more likely to return empty compared to high-strain foragers. These studies demonstrate how a genotypically varied sensory-physiological process, the perception of sucrose, are associated with a division of labor for foraging.