Genetic links illuminate bee social life

How social life evolved from solitary ancestral lifestyles has been an enduring mystery for years, and now scientists are one step closer to unravelling its genetic underpinnings.

In a paper published in the journal PLoS Biology, Arizona State University School of Life Sciences collaborators Gro Amdam, Robert Page and Kate Ihle, together with University of California affiliated Mindy Nelson, have shown that a single gene, vitellogenin, controls multiple aspects of honey bee social organisation.

Vitellogenin encodes for the protein vitellogenin, which is found in most egg laying organisms (there is even a homologous gene family in humans). It was first discovered in honey bees in the 1970s.

That queen bees expressed the protein came as no surprise as they are the dominant egg layers in a hive, but that the protein was also found in the essentially sterile female worker bees caught scientists' interest. However, since no role for it in workers could be found at the time, some speculated that it was simply evolutionary baggage. One of those who didn't agree was Amdam.

"I came out of a mathematical background with emphasis on theoretical regulatory biology," Amdam says. "The models I built on vitellogenin dynamics suggested that worker bees synthesised large amounts per time unit, and since the protein did not accumulate in tissues and blood it was likely metabolised or transferred somewhere else."

In 2002 while Amdam pursued her PhD at the Norwegian University of Life Science, she discovered where that "somewhere else" was. Vitellogenin produced in workers was actually fed to queens and bee larvae as royal jelly.

Thus, a protein believed to be exclusively linked to egg development had changed its job description in sterile bees.

"This was achieved by workers expressing an ovarian vitellogenin receptor on their paired head glands, which are responsible for the making of jelly," she says.

Worker honey bees go through a sequence of tasks as they age. They start out as nest workers that produce jelly, and later turn to foraging for nectar and pollen in the field. Foragers do not produce vitellogenin.

The insight that vitellogenin was important during the nest stage, and thus for worker division of labour, led Amdam to speculate that the protein could - directly or indirectly - affect the bees transition from nest tasks to foraging duties.

"The age at onset of foraging is highly variable, but there was no good physiological model for explaining this variation. One possibility was that the probability of starting foraging was related to the level of the bees' dynamic vitellogenin stores," Amdam says.

"This would ensure that vitellogenin-rich bees stayed in the nest as useful nurses of the brood and other bees, whereas vitellogenin-exhausted bees became foragers."

In a first attempt to address this hypothesis, Amdam and colleagues at the University of Sao Paulo showed that suppression of vitellogenin leads to high titers of juvenile hormone - a systemic hormone associated with foraging activity.

Parallel experiments by Amdam's group in Norway further suggested that vitellogenin could scavenge free radicals and possibly and extend lifespan by reducing oxidative stress damage both workers and queens.

Amdam's curiosity about the switch between nursing to foraging, led her to collaborate with Page who studied the division of labour between nectar and pollen foraging bees. Page's selection program had resulted in honey bee strains that had different foraging preference: one strain preferred nectar, the other pollen.

These strains also differed with regard to the average age of foraging onset. Amdam and Page started to map out their vitellogenin dynamics, first at University of California at Davis, then at ASU when Page became director of the School of Life Sciences. Amdam came to the College of Liberal Arts and Sciences as an assistant professor in life sciences in 2005.

"This collaborative work was all very exciting. Rob and I confirmed that vitellogenin was possibly involved in division of labour (nurse v forager); possibly involved in further division of labour between foragers (as nurse bee pollen specialists have higher vitellogenin levels than future nectar specialists); and possibly affecting the lifespan of workers. These are very central aspects of a worker bee's life history: addressing how they mature and develop behaviourally in the colony, the way they divide labour among them, and how long they live."

The direct linkage between these three aspects of social life histories in bees and the gene, vitellogenin, was solidified in the study published in PLoS Biology through the use of RNA interference (RNAi).

Amdam was the first to adapt this technique for use in adult honey bees and to target vitellogenin. In the study, vitellogenin knockdowns are shown to initiate foraging earlier in life, to show a preference for nectar collection and die more quickly than in control animals.

According to Amdam, all three hypotheses were confirmed in this study. "We now know that vitellogenin paces the behavioural development of bees, it is part of the machinery that determines when they start foraging; it is a primer for the bees subsequent preference for nectar or pollen," she says.

Ihle, a graduate student in both Amdam's and Page's laboratories, and collaborator on this paper adds that RNAi will give them the opportunity to use functional genomics to investigate the overall origins of sociality.

Amdam agrees. "Our work with vitellogenin shows that many of the highly derived social behaviours that people tend to think might be new or novel actually build on the exploitation of a very old gene that is present in reproductive, solitary foremothers."

Source: Arizona State University College of Liberal Arts and Science