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A single molecule can switch an ant from worker to queen

Indian jumping ants are active predators with large jaws. They live in small groups, each one with a queen that lays eggs, and with workers that forage and defend the colony. Unlike most species of social ants, however, there is very little difference in appearance between the workers and the queen. If a queen dies or is removed, the workers have the ability to switch castes and begin laying fertilized eggs like a queen. These queen-like workers are called gamergates.

Although differences in the levels of certain hormones have been associated with switches between worker and gamergate castes, the exact mechanism which underlies caste-specific behavior changes has not been known. 

Now, researchers at the University of Pennsylvania and the University of Freiburg, Germany, have discovered that a single protein, Kr-h1 (Krüppel homolog 1), acts in the brains of both worker ants and gamergates to produce caste-appropriate behavior. In addition, socially regulated hormones are involved in coordinating the complex social transition from worker to gamergate caste. 

“Animal brains are plastic; that is, they can change their structure and function in response to the environment,” said Roberto Bonasio of the University of Pennsylvania Perelman School of Medicine. “This process, which also takes place in human brains – think about the changes in behavior during adolescence – is crucial to survival, but the molecular mechanisms that control it are not fully understood. We determined that, in ants, Kr-h1 curbs brains’ plasticity by preventing inappropriate gene activation.”

Ants in the colony all have the genetic information required to behave in both ways, as a worker or as a queen. Yet, under normal circumstances the ants belong to one caste only and behave in a socially appropriate way for that caste. The workers maintain the colony by finding food and fighting invaders, while the queen’s main task is to lay eggs.  

By studying ants, Bonasio and colleagues wanted to understand how turning certain genes “on” or “off” affects brain function and behavior. Because Harpegnathos adults can switch from a worker to a gamergate, they were perfect study animals. 

In order to investigate the underlying molecular events that cause the switch in behavior, the research team isolated neurons from the ants’ brains and cultured them in the laboratory. They exposed the cultured neuronal tissue to different levels of two hormones, juvenile hormone 3 (JH3) and ecdysone (E20) to see how these hormones affected gene expression in the brain cells. 

The study revealed that the two hormones, which are normally present at different levels in the bodies of workers and gamergates, produced distinct patterns of gene activation in the brains of the two castes. In addition, the experts found that both hormones influenced the cells by activating a single protein, Kr-h1. The hormones directed the transcriptional factor (Kr-h1) to repress the expression of different target genes in the two castes of ants.

In more detailed experiments, the researchers knocked down (silenced) the Kr-h1 protein in ant brains and found that this caused the activation of gamergate genes in workers, and the activation of worker genes in gamergates. This situation led to inappropriate behavior by ants and a destabilization of caste identity.

“This protein regulates different genes in workers and gamergates and prevents the ants from performing ‘socially inappropriate’ behaviors,” said study co-author Shelley Berger. “That is to say, Kr-h1 is required to maintain the boundaries between social castes and to ensure that workers continue to work while gamergates continue to act like queens.”

“We had not anticipated that the same protein could silence different genes in the brains of different castes and, as a consequence, suppress worker behavior in gamergates and gamergate behavior in workers,” added Bonasio. “We thought that these jobs would be assigned to two or more different factors, each of them only present in one or the other brain.”

The findings establish that socially important hormones and gene regulation are at the basis of the ability of animal brains to switch from one genetic mode and social caste to another. 

“The key message is that, at least in ants, multiple behavioral patterns are simultaneously specified in the genome and that gene regulation can have a great impact on which behavior that organism carries out,” said Berger. “In other words, the parts of both Dr. Jekyll and Mr. Hyde are already written into the genome; everyone can play either role, depending on which gene switches are turned on or off.”

The researchers think the implications may go much further than understanding behavioral plasticity in ants and other insects. “It is tempting to speculate that related proteins might have comparable functions in more complex brains, including our own,” said Bonasio. “Discovering these proteins might allow us to one day restore plasticity to brains that have lost it, for example aging brains.”

The research is published today in the journal Cell.

By Alison Bosman, Staff Writer

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