Individuals with well-defined roles can be driven to perform jobs outside their areas of expertise by changes in the environment. We know many animals can make these shifts but, in large part, we know very little about the genetic/molecular basis of environmentally induced switches in behavior. Christophe Lucas and Marla Sokolowski from the University of Toronto recently took on this question by studying shifts in social behavior in the ant, Pheidole pallidula. They published their work in a recent edition of the Proceedings of the National Academy of Sciences.
Pheidole pallidula colonies consist of morphologically and behaviorally specialized castes: minors (`foragers') and majors (`soldiers'). But individuals can switch jobs at a pinch. If the colony comes under attack,foragers will do some `soldiering'; likewise, if the colony stumbles on a new food source, soldiers will help out with the harvest.
To get at the molecular underpinnings of this switch, Lucas and Sokolowski first looked for forager, a gene involved in controlling how Drosophila search for food. The team found a closely related gene in P. pallidula (ppfor) that codes for the enzyme cGMP-dependent protein kinase (PKG). The enzyme is in the brains of both castes, but is only expressed in a small subset of cells. Intriguingly, when the team assayed PKG activity in brain tissue, they found that soldiers have more PKG activity than foragers. PKG activity is clearly correlated with being a soldier ant.
The team next tested how environmental cues affect PKG activity. First,they gave ants a cue to stimulate foraging (a live mealworm). Afterwards, both soldiers and foragers showed reduced PKG activity when compared with controls(animals who had only encountered a plastic mealworm). In a converse experiment, the team gave ant colonies a cue designed to stimulate defensive behaviors. They placed an `intruder ant' in an enclosure within the nest. The presence of the intruder caused PKG activity to rise in both castes.
The team's initial experiments provided solid evidence that PKG activity is down-regulated during foraging and up-regulated during colony defense. So is PKG activity alone sufficient to make ants more defensive? To address this,the team spiked colony food with a PKG activator drug, then watched how ants responded to foraging (mealworm) and defensive (alien intruder) stimuli. Indeed, when the insects' PKG levels were elevated, both castes were less interested in foraging, and soldiers spent more time in defensive mode when presented with an intruder.
Lucas and Sokolowski have been able to causally link a single gene product in a small population of brain cells to a complex shift in social behavior. They were able to do this, in large part, because of the unique specializations and behavioral repertoire of ants. As such, this work stands out as an example of how studying social insects can offer unique opportunities to address questions that are often difficult to get traction on in other animals.
This work is also notable because it represents the application of Sokolowski's decades of molecular/genetic expertise in Drosophila to a new animal – one with an added dimension of social behavior not seen in fruit flies. Roving out into new territory like this is not an easy thing for a researcher to do, but Lucas and Sokolowski's work shows that the approach can pay off.
