Genomic dissection of behavioral maturation in the honey bee

Abstract

Honey bees undergo an age-related, socially regulated transition from working in the hive to foraging that has been previously associated with changes in the expression of thousands of genes in the brain. To understand the meaning of these changes, we conducted microarray analyses to examine the following: (i) the ontogeny of gene expression preceding the onset of foraging, (ii) the effects of physiological and genetic factors that influence this behavioral transition, and (iii) the effects of foraging experience. Although >85% of Ϸ5,500 genes showed brain differences, principal component analysis revealed discrete influences of age, behavior, genotype, environment, and experience. Young bees not yet competent to forage showed extensive, age-related expression changes, essentially complete by 8 days of age, coinciding with previously described structural brain changes. Subsequent changes were not age-related but were largely related to effects of juvenile hormone (JH), suggesting that the increase in JH that influences the hive bee-forager transition may cause many of these changes. Other treatments that also influence the onset age of foraging induced many changes but with little overlap, suggesting that multiple pathways affect behavioral maturation. Subspecies differences in onset age of foraging were correlated with differences in JH and JH-target gene expression, suggesting that this endocrine system mediates the genetic differences. We also used this multifactorial approach to identify candidate genes for behavioral maturation. This successful dissection of gene expression indicates that, for social behavior, gene expression in the brain can provide a robust indicator of the interaction between hereditary and environmental information. T he honey bee, Apis mellifera, is one of the model organisms being used to achieve a comprehensive understanding of social life in molecular terms: how social life evolved, how it is governed, and how it influences all aspects of genome structure, genome activity, and organismal function (1). Honey bees offer complex but experimentally accessible social behavior, a compact and well studied brain, and a sequenced genome that provides the foundation for ever-increasing genomic resources.Honey bees, like many species of social insects, display a division of labor among colony members that is based on behavioral specializations associated with age (2). Adult worker honey bees perform a series of tasks in the hive when they are young (such as brood care or ''nursing'') and, at Ϸ2-3 weeks of age, shift to foraging for nectar and pollen outside the hive. The transition to foraging involves changes in endocrine activity, metabolism, circadian clock activity, brain chemistry, brain structure, and brain gene expression (3).The pace of behavioral maturation in honey bees is not rigid, because the onset age of foraging depends on the needs of the colony. Pheromones and other social cues mediate this behavioral ontogeny and affect foraging onset (4). These cues are thought to act direct...

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

“…Energy metabolism genes were enriched among genes regulated by methoprene in the brain, but they were up-regulated (Table 1). This result is in contrast to the finding that methoprene causes forager-like changes in overall brain gene expression (36,37). QMP causes nurse-like overall changes (36) but did not affect brain energy metabolism gene expression (Table 1).…”

“…The list of genes differentially expressed in the brains of nurses and foragers was not significantly enriched for energy metabolism genes (37). However, differentially expressed energy metabolism genes were predominantly up-regulated in nurse bees (Table 1), including five of six in the citrate cycle (Fig.…”

“…We obtained additional evidence for atypical regulation of insulin signaling by annotating energy metabolism pathways with results from three previously published microarray experiments (36,37). These experiments produced three lists of genes that were differentially expressed: (i) in the brains of nurse bees and foragers; (ii) in response to methoprene, which accelerates the onset age of foraging (23); and (iii) in response to queen mandibular pheromone (QMP), which delays the onset age of foraging (38).…”

“…Insulin signaling both regulates and is regulated by changes in energy metabolism, and generally there is a positive correlation between insulin signaling and energy metabolism gene expression in a variety of species and tissues (39 -41). To test whether this positive relationship is present in the honey bee brain, we mapped genes to conserved energy metabolism Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways (42) and performed statistical tests for enrichment and directional bias on each list of genes generated by the microarray experiments (37).…”

The transcriptomic and evolutionary signature of social interactions regulating honey bee caste development

“…2000), as well as the composition of nurse glandular secretions (Haydak 1970), and patterns of nurse brain gene expression (Whitfield et al. 2006) all vary with nurse age and social environment. While it is not clear how exactly these differences are related to the observed differences in nurse provisioning behavior, individually marked nurses did tend to specialize on feeding either queen or worker cells within a day, but not across multiple days.…”