Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.

Honey bees (Apis mellifera) provide a system for studying social and food-related behavior. A caste of workers performs age-related tasks: young bees (nurses) usually feed the brood and other adult bees inside the nest, while older bees (foragers) forage outside for pollen, a protein/lipid source, or nectar, a carbohydrate source. The workers' transition from nursing to foraging and their foraging preferences correlate with differences in gustatory perception, metabolic gene expression, and endocrine physiology including the endocrine factors vitellogenin (Vg) and juvenile hormone (JH). However, the understanding of connections among social behavior, energy metabolism, and endocrine factors is incomplete. We used RNA interference (RNAi) to perturb the gene network of Vg and JH to learn more about these connections through effects on gustation, gene transcripts, and physiology. The RNAi perturbation was achieved by single and double knockdown of the genes ultraspiracle (usp) and vg, which encode a putative JH receptor and Vg, respectively. The double knockdown enhanced gustatory perception and elevated hemolymph glucose, trehalose, and JH. We also observed transcriptional responses in insulin like peptide 1 (ilp1), the adipokinetic hormone receptor (AKHR), and cGMP-dependent protein kinase (PKG, or “foraging gene” Amfor). Our study demonstrates that the Vg–JH regulatory module controls changes in carbohydrate metabolism, but not lipid metabolism, when worker bees shift from nursing to foraging. The module is also placed upstream of ilp1, AKHR, and PKG for the first time. As insulin, adipokinetic hormone (AKH), and PKG pathways influence metabolism and gustation in many animals, we propose that honey bees have conserved pathways in carbohydrate metabolism and conserved connections between energy metabolism and gustatory perception. Thus, perhaps the bee can make general contributions to the understanding of food-related behavior and metabolic disorders. Communication between internal energetic state and taste perception helps animals control food uptake and maintain normal life functions. Honey bees provide an animal model for studies of food-related behavior, such as the role of taste sensitivity in choice-making between carbohydrate- and protein-rich foods (nectar versus pollen for honey bees). A young bee's taste sensitivity to sugar predicts when she begins foraging later in life and influences her choice of foods. Vitellogenin (Vg), a protein produced in the bee's fat cells, and juvenile hormone (JH) influence honey bee taste perception and food-related behavior. Vg and JH are connected by a feedback loop, and we perturbed this Vg–JH circuit using a double gene knockdown approach. In response, bees became more sensitive to sugar, had higher sugar levels in the blood, and died faster during starvation, while lipid levels remained constant. We identified that insulin like peptide 1 (ilp1), the adipokinetic hormone receptor (AKHR), and PKG (the foraging gene) were altered in the bees' fat cells after the perturbation. Our study demonstrates a new role for the Vg–JH circuit in honey bee carbohydrate metabolism, and it places Vg–JH upstream of the three metabolic genes that have conserved roles in food-related behaviors and energy metabolism in many animals.

Animal structures occasionally attain extreme proportions, eclipsing in size the surrounding body parts. We review insect examples of exaggerated traits, such as the mandibles of stag beetles (Lucanidae), the claspers of praying mantids (Mantidae), the elongated hindlimbs of grasshoppers (Orthoptera: Caelifera), and the giant heads of soldier ants (Formicidae) and termites (Isoptera). Developmentally, disproportionate growth can arise through trait-specific modifications to the activity of at least four pathways: the sex determination pathway, the appendage patterning pathway, the insulin/IGF signaling pathway, and the juvenile hormone/ecdysteroid pathway. Although most exaggerated traits have not been studied mechanistically, it is already apparent that distinct developmental mechanisms underlie the evolution of the different types of exaggerated traits. We suggest this reflects the nature of selection in each instance, revealing an exciting link between mechanism, form, and function. We use this information to make explicit predictions for the types of regulatory pathways likely to underlie each type of exaggerated trait.

SUMMARY: Rearing oxygen level is known to affect final body size in a variety of insects, but the physiological mechanisms by which oxygen affects size are incompletely understood. In Manduca sexta and Drosophila melanogaster, the larval size at which metamorphosis is initiated largely determines adult size, and metamorphosis is initiated when larvae attain a critical mass. We hypothesized that oxygen effects on final size might be mediated by oxygen effects on the critical weight and the ecdysone titers, which regulate growth rate and the timing of developmental transitions. Our results showed that oxygen affected critical weight, the basal ecdysone titers and the timing of the ecdysone peak, providing clear evidence that oxygen affected growth rate and developmental rate. Hypoxic third instar larvae (10% oxygen) exhibited a reduced critical weight, slower growth rate, delayed pupariation, elevated baseline ecdysone levels and a delayed ecdysone peak that occurred at a lower larval mass. Hyperoxic larvae exhibited increased basal ecdysone levels, but no change in critical weight compared with normoxic larvae and no significant change in timing of pupariation. Previous studies have shown that nutrition is crucial for regulating growth rate and the timing of developmental transitions. Here we show that oxygen level is one of multiple cues that together regulate adult size and the timing and dynamics of growth, developmental rate and ecdysone signaling.