ABOVE: A Harpegnathos saltator worker guards a brood composed of eggs and different stages of larvae. Karl Glastad, Berger Lab

Indian jumping ants (Harpegnathos saltator) are unusual in that worker ants can, in the absence of a queen, make a switch to a queen-like status in order to reproduce and keep the colony going. In a study published November 4 in Cell, researchers found that the shift from worker to queen is facilitated by the response of transcription factor Krüppel homolog 1 (Kr-h1) to hormones that are present at different levels in queen and worker ants.

“As a field, we’re very interested in understanding the evolution of sociality,” says Tali Reiner Brodetzki, who studies social behavior in ants at Rutgers University–Camden in New Jersey and was not involved in the work. Most social insects can’t change their caste, she adds, but studying this plasticity could yield insights into how other types of plasticity work.

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Previous work has shown that Indian jumping ants can change the size of their brains depending upon whether they’re workers or queens—a transition that happens during a tournament of sorts in which workers dubbed gamergates fight each other for the chance to become the acting queen. In 2020, Roberto Bonasio’s group at the University of Pennsylvania showed that the ants can expand their glial cells when making the transition from worker to queen. “Because they have such pronounced differences between their behaviors” that are also reflected physically in the brain, he explains, “the ants are ideal to study how turning on or off certain genes can affect ingrained patterns of behavior.”

In the new study, Bonasio and colleagues analyzed gene expression in the brains of H. saltator workers and queens and identified 2,540 transcripts with differential expression between the two. Based on prior work, they looked for downstream targets of two hormones—ecdysone, which is known to be increased in queens, and juvenile hormone, which has been associated with workers—and found that three of the most upregulated genes in the brains of worker ants have been linked with juvenile hormone signaling. Ecdysone appeared to affect levels of gene expression in the brains of queens, including three so-called ecdysone-induced protein genes.

When artificially delivered to the brains of 10-day-old ants, juvenile hormone produced worker-like ants and ecdysone resulted in queen-like ants, as defined by both gene expression patterns and behavior.

The researchers also cultured the ants’ neurons and administered each hormone to take a deeper dive into gene expression changes. In doing so, they determined that the Kr-h1 transcriptional repressor is activated by both hormones. Depending on which hormone it is responding to, Kr-h1 binds to either queen- or worker-associated gene promoters and represses transcription of those genes. It’s not yet clear how Kr-h1 manages to regulate two context-dependent sets of transcripts, but the authors hypothesize that different isoforms of Kr-h1 may be induced by each hormone, and that proteins that interact with Kr-h1 and differences in chromatin structure around the two types of genes may be involved.

“The biggest question is, how much is this specific to the ants and how much does it go well beyond?” Bonasio says. “I strongly believe—and history is on my side, in biology at least—that a lot of these mechanisms will be conserved, and, if you look hard enough, you will see them also in other organisms.”

It’s already known that juvenile hormone, ecdysone, and Kr-h1 “seem to be common players across ant species, but how they’re utilized is different in different ants, bees, and wasps,” explains Adria LeBoeuf, a neuroscientist studying social and collective behavior at the University of Fribourg in Switzerland who did not participate in the work. For instance, juvenile hormone has been shown to be influential during ant development and the formation of social castes. The results here reinforce that “all of these major insect hormones are very tangled,” she says.

This leads to several open questions, LeBoeuf adds. “Somehow these hormones end up in the brain, [but] we don’t know how they get there,” she says, or why they regulate specific genes and not others. In the future, more exploration of the pathways involved and how those pathways affect downstream behavior from within and outside the brain—in the ovaries, for instance, which grow during the transition from worker to queen—will be important, she adds. “Genomics is more at our fingertips, but I think physiology is where it’s at for are getting the answers that we need to understand how the system works.”

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