Study identifies molecular changes that reshape aging and behaviour in infected workers, leading to a partially queen-like phenotype

A tapeworm fundamentally changes the lives of ants: Workers of the species Temnothorax nylanderi that are infected with the tapeworm Anomotaenia brevis live several times longer than their uninfected nestmates. They are also less active, while their metabolism becomes partly more similar to that of queens. A new study by Johannes Gutenberg University Mainz (JGU), now published in the journal BMC Genomics, reveals the molecular basis of this unusual effect.

The researchers found evidence that the parasite alters existing biological programs in the ant. For the tapeworm, this change could be advantageous, as the ants serve as intermediate hosts. The parasite only develops fully in woodpeckers, its definitive hosts. The fact that infected workers live longer and are less active could promote its transmission.

For the study, the team led by Professor Susanne Foitzik from the Institute of Organismic and Molecular Evolution (iomE) at JGU examined ants from the Lenneberg Forest near Mainz. In the laboratory, these were assigned to three groups: queens, workers infected with the tapeworm, and uninfected workers. From the ants, the researchers dissected the brain and the fat body, a tissue in the abdomen that is important, among other things, for metabolism and the immune system. They then used RNA sequencing to analyze which genes were active in the brains and fat bodies. In addition, they examined genome and transcriptome data from the tapeworm, meaning data on its genetic material and on the genes that are active in it. This allowed them to test whether the parasite mimics the ants’ own signaling molecules.

Infection alters ant physiology in a targeted way

“Our genetic analyses show that the infection does not simply make the ants sick, but alters their physiology in a highly targeted way,” said Susanne Foitzik. “At the molecular level, infected workers showed a profile that was partially queen-like.” This was particularly clear in the fat body. “There, we found clear overlaps between infected workers and queens.” The affected genes included genes linked to metabolism, the immune system, stress resistance, and aging processes.

“The findings in the fat body suggest that the tapeworm taps into existing signaling and metabolic pathways of the ant and shifts them,” said Foitzik. This finding is particularly interesting for the aging of the animals: Earlier studies of this ant-tapeworm system have shown that infected workers have survival rates approaching those of queens. Queens of this species can live for up to 20 years, while workers usually live only one to two years. The fact that infected workers show a partly queen-like molecular profile in the fat body could help explain this effect.

Dampened signals in the brain

The picture was different in the brain. There, infected workers were much less similar to queens. Instead, many neuropeptides, signaling molecules that can influence behavior, feeding, and social responses, as well as their receptors, were downregulated. The altered activity of these signaling pathways could help explain why infected workers show less worker-like behavior.

“The effect of the infection is therefore tissue-specific,” explained Giulia Blasi, first author of the study and a doctoral researcher at iomE. “In the fat body, we see a shift toward a queen-like metabolic profile. In the brain, by contrast, many signaling pathways linked to behavior and activity are dampened.”

One possible explanation would have been that the tapeworm mimics ant signaling molecules by producing its own neuropeptides that resemble those of the ants and thus trick the ants’ signaling system. However, the researchers found no evidence for this, as the peptides produced by the parasite were not sufficiently similar to those of its host. “The data rather suggest that the parasite influences the ant indirectly by intervening in the host’s own regulatory networks, which control metabolism, the immune system, aging, and behavior, among other processes,” said Blasi.

Model for parasitic manipulation

“Queens and workers of social insects share the same genetic basis, but differ greatly in lifestyle and lifespan,” said Susanne Foitzik. “The fact that infected workers show a partly queen-like molecular profile in the fat body suggests that the parasite taps into existing biological programs of the ant.” The ant-tapeworm system therefore provides a suitable model for investigating how parasites can alter the aging and behavior of their hosts.

The study was funded by the German Research Foundation. Susanne Foitzik, Giulia Blasi, and Katharina Schwolow from JGU, as well as Hugo Darras from Zhejiang University in Hangzhou, China, were involved in the project.