A team of researchers from Arizona State University, Purdue University and the Norwegian University of Life Sciences has discovered evidence that honeybees have adopted a phylogenetically old molecular cascade – TOR (target of rapamycin), linked to nutrient and energy sensing – and put it to use in caste development. Effect of rapamycin/FK506 pharmacology on caste characters in honey bees (Vehicle = 2% ethanol in insect saline; FK+R = sequential treatment of FK506, rapamycin; R = rapamycin; W = worker as comparison). In queen-destined individuals, rapamycin: a, prolonged development and b, reduced wet-weight (size) at adult emergence; c, ovary size was not affected by pharmacology but rapamycin d, induced the worker-specific trait corbicula (arrow in top panel shows location on hind leg); pictures of hind leg basitarsus covered with short hairs in Vehicle and FK+R, and by long corbicular hairs (e.g. arrows) in R and W (scale bar 0.25 mm). Corbicula is associated with low basitarsus length/width ratio , and in accord R individuals showed a decrease in this Basitarsal Index (BI) mean±s. e. noted in d (ANOVA: F3,21 = 21.48, P<0.00001, Fisher LSD: P<0.00001; vs. between Vehicle and FK+R controls and between worker-destined groups P>0.50). e–g, rapamycin/FK506 pharmacology did not affect worker-destined bees. Bars are means±s. e. (asterisk P<0.02, two asterisks P<0.005, three asterisks P<1.0 10−6). oi:10.1371/journal.pone.0000509.g001
The findings show that TOR is directly linked in the nutrient-induced development of female honeybees into either queens, the caste of large dominant egg-layers, or into workers, the caste of small helpers.
“Our study provides three independent lines of evidence – gene expression, pharmacology and RNA interference (RNAi) – that converge on one conclusion: selection can have acted on the TOR pathway to enable two distinct phenotypes to evolve in the bee,” says Gro Amdam, an assistant professor in ASU’s School of Life Sciences.
The researchers found that queen-fate can be blocked, and that workers develop, when TOR activity is reduced during development.
Amdam notes that while social insect queens and workers have been subjects of great fascination for centuries, and scientific study for the last few decades, the gene regulatory pathways responsible for determining caste fate has remained largely unknown. This is the first time a genetic pathway has been identified to control these two phenotypes, says Amdam, who heads social insect studies in laboratories at both ASU and the Norwegian University Department of Animal and Aquacultural Sciences.
“The finding that queens and workers can emerge from an old pathway that controls tissue growth in a variety of species, including humans, helps us understand what evolution builds on when it produces seemingly radically new phenotypes,” Amdam says.
In addition to Amdam, researchers reporting these findings include: Avani Patel, M. Kim Fondrk, Osman Kaftanoglu and Katy Frederick of ASU, and Christine Emore and Greg Hunt of Purdue University’s Entomology Department.