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

Abstract

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.

Glossary of terms: Words rendered in bold font in the body of the text are defined here.

Bioinformatics

The use of computational techniques to manage and analyze large quantities of information from biological systems, predominantly genomic and transcriptomic data (Hogeweg 2011).

Caste

Term used to describe a group of individuals in social insect colonies that specializes, to some extent, in specific occupations as a result of division of labor. Social insect castes can be associated with differences in age, anatomy, and morphology.

cis-regulatory elements

A sequence of DNA which, via the binding of transcription factors or other proteins, regulates the expression of a gene or genes on the same chromosome (Wray 2007).

Division of labor

A social system in which individuals specialize in specific occupations. In insect societies, queens mostly reproduce, whereas workers engage in all tasks related to colony growth and development. Young workers tend to work in the nest, whereas older individuals forage outside the nest.

DNA methylation

A form of epigenetic modification in which methyl groups are attached to nucleotides, usually CpG dinucleotides, have the potential to affect the expression of methylated sequences (Bird 2007).

Epigenetics

Environmental mediation of an individual’s genome and/or its descendants, without changes in DNA sequence, via mechanisms like DNA methylation and histone modification (Crews 2008).

Eusocial

Traditionally defined as social species that show three features: extreme asymmetries in reproduction, with some individuals reproducing a great deal and others little or not at all; overlapping generations of adults in the nest; and cooperative care of offspring (Wilson 1971).

Expressed sequence tags (EST)

ESTs are produced by sequencing many clones from cDNA libraries; since the sequences from these cDNA libraries are originally derived from mRNA from the organism of interest, ESTs provide important information regarding what genes are being expressed (Gerhold and Caskey 1996).

Genome

The complete genetic code for an organism.

Genetic toolkit

The concept that conserved genes and pathways have similar roles across a variety of taxa, helping to “build” different phenotypes from the same “tools,” resulting in diverse phenotypes regulated by similar factors (Toth and Robinson 2007).

Insulin/insulin-like signaling (IIS)

Metabolic pathway that acts as a key regulator of growth, feeding behavior, and metabolism; in insects, it also interacts with target of TOR and JH (Edgar 2006, Tu et al. 2005).

Juvenile hormone (JH)

Insect hormone involved in many behavioral and developmental processes, including onset of foraging behavior in honey bees (Hartfelder 2000).

Microarray

Technology that allow for the quantification of gene expression via the hybridization of cDNA to complementary sequences on a chip (Schena et al. 1995), used in conjunction with ESTs to quantify known genes.

MicroRNA

A small section of noncoding RNA that has transcriptional and posttranslational effects on gene expression (Chen and Rajewsky 2007).

Quantitative trait loci (QTL)

Sections of DNA sequence (loci) that contain or are linked to quantitative trait. QTLs can also be mapped to whole or partial genomes to further identify genes associated with the trait of interest (Erickson et al. 2004).

Queen mandibular pheromone (QMP)

Pheromone produced by honey bee queens to regulate the behavior and reproductive physiology of workers (Winston and Slessor 1998).

RNA-Seq

A form of transcriptomic profiling where high-throughput sequencing of all the cDNA contained in a sample provides precise measurements of gene expression (Wang et al. 2009).

Single-cohort colonies

Behavioral manipulation in which hives are created solely from young workers. This modification of normal age demography results in newly formed colonies that lack foragers, and young workers subsequently transition to foraging behaviors earlier than normal, allowing researchers to compare same-aged individuals that perform different tasks (Nelson 1927; Robinson et al. 1989).

Target of rapamycin (TOR)

An important metabolic regulator that interacts with the IIS pathway (Tu et al. 2005).

Transcription factor

A protein that binds to a regulatory DNA segment, regulating the transcription of specific target genes into mRNA.