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Single-Nucleus Sequencing Analysis Generates Cell Atlas of Ant Superorganism Brains

NEW YORK — Researchers have generated a single-cell atlas of pharaoh ant brains, giving a glimpse into their social division of labor.

Ant colonies have been thought of as a type of superorganism, as different members — workers, queens, males, or unfertilized gynes that develop into queens — have specific jobs, suggesting that their brains could also have adapted to their particular functions.

A BGI-Research-led team generated transcriptomes for more than 200,000 single nuclei isolated from the brains of pharaoh ants, Monomorium pharaonis. As they reported on Thursday in Nature Ecology & Evolution, the researchers found the brains of worker and male ants to be highly specialized and further noted transcriptomic changes in the brains of gynes as they transformed into queens.

"Our discoveries suggest that functional specialization of their brains appears to be a mechanism underlying the social task division among individual ants," first author Qiye Li, a researcher at BGI-Research, said in a statement. "We humans learn and train ourselves to do different jobs, while ants are born with a specific role in their colony."

The researchers conducted whole-brain single-nucleus sequencing of four gyne, four queen, four male, and five worker ants. For each type of ant, they generated data on an average of 50,000 nuclei, for a total of 206,367 nuclei.

Based on gene expression patterns, these nuclei clustered into 43 groups, many of which the researchers could annotate based on marker genes from Drosophila and hymenopteran species. They could, for instance, identify Kenyon cells, olfactory projection neurons, and ensheathing glia. They further annotated optic lobe cell types for which marker genes are lacking based on similar to orthologous genes in Drosophila and Harpegnathos saltator, a type of ant found in India.

Nearly all of the cell types the researchers identified were present among the M. pharaonis ant castes, but they were present in varying amounts.

Queens and gynes, for instance, had largely generalized cell compositions. For many ants, queens may retain a generalist function, as they have to strike out on their own to form a new colony, though M. pharaonis queens do not do that. Still, the researchers said that M. pharaonis queens do sometimes fail to become inseminated and then perform more worker-like behaviors.

At the same time, they noted that queens have lower levels of optic lobe cell types, suggesting that vision-related functions may have degenerated in them as they spend most of their time in the dark inner nest.

Worker ants, which are female, and male ants were more specialized. Worker ants had higher portions of Kenyon cells and olfactory projection neurons, but lower levels of optic lobe neurons. Male ants, by contrast, featured the opposite pattern.

These differences are consistent with the ants' social and sexual specializations. Worker ants are responsible for all the tasks of the ant colony other than reproduction and need brains that handle those various tasks, as reflected by Kenyon cells and olfactory projection neurons that process complex information. Male ants, though, only have one function of finding and inseminating a virgin queen.

The researchers also noted a change in the proportion of cell types among gynes upon insemination. For instance, one cell cluster that expresses higher levels of ple and DAT, both of which indicate the involvement of dopaminergic neurons, became more predominant. Based on this, the researchers treated a portion of M. pharaonis gynes with L-Dopa to find that it led them to have more yolky oocytes, suggesting a gonadotrophic role for dopamine. They further found that dopamine likely has its gonadotrophic effect through the Dh31-expressing neurons found in another cluster.

"This study helps us understand the complexity of ant brains and how the complementary specialization in brains enables ants within a colony to function as a superorganism," co-corresponding author Guojie Zhang from Zhejiang University said in a statement.

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