Behavioral genomics of honeybee foraging and nest defense

Abstract

The honeybee has been the most important insect species for study of social behavior. The recently released draft genomic sequence for the bee will accelerate honeybee behavioral genetics. Although we lack sufficient tools to manipulate this genome easily, quantitative trait loci (QTLs) that influence natural variation in behavior have been identified and tested for their effects on correlated behavioral traits. We review what is known about the genetics and physiology of two behavioral traits in honeybees, foraging specialization (pollen versus nectar), and defensive behavior, and present evidence that map-based cloning of genes is more feasible in the bee than in other metazoans. We also present bioinformatic analyses of candidate genes within QTL confidence intervals (CIs). The high recombination rate of the bee made it possible to narrow the search to regions containing only 17-61 predicted peptides for each QTL, although CIs covered large genetic distances. Knowledge of correlated behavioral traits, comparative bioinformatics, and expression assays facilitated evaluation of candidate genes. An overrepresentation of genes involved in ovarian development and insulin-like signaling components within pollen foraging QTL regions suggests that an ancestral reproductive gene network was co-opted during the evolution of foraging specialization. The major QTL influencing defensive/aggressive behavior contains orthologs of genes involved in central nervous system activity and neurogenesis. Candidates at the other two defensive-behavior QTLs include modulators of sensory signaling (Am5HT(7) serotonin receptor, AmArr4 arrestin, and GABA-B-R1 receptor). These studies are the first step in linking natural variation in honeybee social behavior to the identification of underlying genes.

Fig. 1

Genetic and phenotypic associations involved in foraging division of labor. Arrows indicate significant correlations between phenotypic traits at the levels of behavior, hormonal signaling, and development and associations between traits and genotypes at specific QTLs (pln 1–4). Colored lines indicate relative titers of specific hormones. The picture illustrates a method for determining the threshold concentration of sugar that a bee will respond to by extending its proboscis or tongue

Fig. 2

QTLs were mapped based on the amount of pollen stored in combs of colonies and confirmed based on individual behavior. Solid bars represent linkage groups with markers. Markers used in confirmation studies are shown. Orthologs of fly genes are indicated with arrows. Dashed lines indicate 97% CIs. Sequenced markers are underlined. No figure is shown for pln-4 because it was mapped by association to one marker (AmFOR) rather than by interval mapping. aPln-1 Map on the left is the localization of the QTL based on colony pollen stores. Map on the right is based on response thresholds to sucrose of individual worker bees. bPln-2QTL map on the left is based on colony pollen stores in a cross between European strains and the map on the right is based on a European by African strain cross. cPln-3QTL map is based on colony pollen stores

Fig. 3

Genetic and phenotypic correlations in defensive responses and specific QTLs. Arrows indicate significant associations between QTL genotypes and behavioral traits and between individual guarding behavior and colony stinging response

Fig. 4

Hypothetical regulatory network influencing honeybee pollen foraging behavior modulated by insulin-like signaling and its effects on ovarian development. Inhibitory blue arrows bridging IIS with the reproductive physiology and hormonal dynamics of the honeybee denote the unique and mutually suppressive feedback interaction between vitellogenin and JII. This interaction is mediated via the allatoregulatory system (Guidugli et al. , and references therein), which includes the IIS pathway (Flatt et al. 2005). ILPs Insulin-like peptides; PI phosphoinositol; PIP phosphoinositol phosphate; IRS insulin receptor substrate gene; PI3K phosphoinositide-3 kinase (class I or II); PIP5K 1-phosphatydylinositol-4-phosphate 5-kinase; PIG-P phosphatidylinositolglycan-peptide; PDK1 3-phosphoinositide-dependent kinase 1; PKB protein kinase B; HR46 honeybee ortholog of Dmel/HR46; PTEN phosphatidylinositol-3,4,5-trisphosphate 3-phosphatase; JH juvenile hormone

Fig. 5

Defensive-behavior QTLs were mapped based on the stinging response of colonies derived from crosses involving haploid drones of a F₁ queen (European×African) each backcrossed to a European queen. Markers used for confirmation studies are indicated. Letters and numbers next to vertical bar represent linked markers. Sequenced markers are underlined. Dashed lines indicate approximate 97% CIs. Approximate positions of honeybee orthologs to Drosophila genes are indicated. a Sting-1. b Sting-2. c Sting-3