Expression profiles during honeybee caste determination

Abstract

Background: Depending on their larval environment, female honeybees develop into either queens or workers. As in other polyphenisms, this developmental switch depends not on genomic differences between queens and workers but on the differential expression of entire suites of genes involved with larval fate. As such, this and other polyphenic systems can provide a novel tool for understanding how genomes and environmental conditions interact to produce different developmental trajectories. Here we use gene-expression profiles during honeybee caste determination to present the first genomic view of polyphenic development.

Results: Larvae raised as queens or workers differed greatly in their gene-expression patterns. Workers remained more faithful than queens to the expression profiles of younger, bipotential, larvae. Queens appeared to both downregulate many of the genes expressed by bipotential larvae and turn on a distinct set of caste-related genes. Queens overexpressed several metabolic enzymes, workers showed increased expression of a member of the cytochrome P450 family, hexameric storage proteins and dihydrodiol dehydrogenase, and young larvae overexpressed two putative heat-shock proteins (70 and 90 kDa), and several proteins related to RNA processing and translation.

Conclusions: Large differences in gene expression between queens and workers indicate that social insect castes have faced strong directional selection pressures. Overexpression of metabolic enzymes by queen-destined larvae appears to reflect the enhanced growth rate of queens during late larval development. Many of the differently expressed genes we identified have been tied to metabolic rates and cellular responses to hormones, a result consistent with known physiological differences between queen and worker larvae.

Figure 1

Cluster analyses showing expression patterns by gene and larval group. Pink, young bipotential larvae; green, worker-destined larvae; blue, queen-destined larvae. Green cells represent relatively low levels of expression, dark gray cells represent moderate expression levels, and red cells represent higher expression. Bars to the left of the array reflect boundaries of genes with relatively high expression in queens (blue), workers and young larvae (pink and green) and workers alone (green).

Figure 2

Proportional expression levels of specific genes. (a) Genes with high expression in young larvae (Y). (b) Genes with high expression in worker larvae (W). (c) Genes with high expression in queen larvae (Q). Normalized expression levels are shown, with standard error bars. FABP is a fatty-acid-binding protein and 52A9 is an oxidoreductase.