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Caste differentiation in ants: How a specific hormone regulates the process

Scientists from the University of Copenhagen have revealed how a specific hormone regulates ant caste differentiation by phenotypic measurements of organ-level developmental changes and matching transcriptome analyses. Published in the Proceedings of the National Academy of Sciences, the titled "Juvenile hormone as a key regulator for asymmetric caste differentiation in ants" significantly enhances the understanding of caste development and evolution.

Most ants have two morphologically differentiated adult castes—queens and workers—each irreversibly specialized for either reproduction or nonreproductive altruism such as foraging, defense and care of maternal brood. Adult gynes (virgin queens) normally have higher body mass, wings and frontal eyes, as well as enlarged ovaries and a sperm storage organ.

In contrast, workers are wingless females with smaller body size and degenerated reproductive tracts, usually without a sperm storage organ. In 1910, the American entomologist William Morton Wheeler noted in his monograph Ants that the superorganismal colonies of ants are strikingly analogous to metazoan bodies because queen and workers function as germline and soma at a higher level of bodily organization: the colony-level.

We are very used to the idea that germline cells in an animal body are set aside for their special reproductive roles very shortly after an egg is fertilized and starts to develop into an embryo. In most social insects with distinct queen (colony germline) and worker (colony soma) castes, the analogous developmental differentiation happens in the larval stage and can still be hormonally reversed.

However, in some ant colonies, germlines are also determined earlier, in the embryonic (egg) stage, begging the question whether that makes somatization of workers as irreversible as somatization of animal body cells as development proceeds.

The new study from the Department of Biology at the University of Copenhagen finds that caste development is remarkably reversible in pharaoh ants, Monomorium pharaonis, a species where caste determination happens in the eggs stage.

"We fed 237 pharaoh ant worker larvae with controlled doses of juvenile hormone (JH) analog during the 3rd larval instar, the final stage of larval development," says Ruyan Li, the lead author of this study.

"We found that hormone-treated worker ants developed many gyne-like physical characteristics, such as increased body length, three extra frontal eyes, wings and flight muscles, gyne-like brains; they even developed the gyne-specific sperm storage organ that workers of this species never have."

However, unlike naturally developed gynes, JH-treated workers never developed ovaries, the reproductive organ that ultimately sets gynes apart from workers, showing that the caste-specific JH-sensitivity window does not overlap with the egg-stage. The study also sheds new light on how shifts in developmental-sensitivity for growth hormone may have played a role in the emergence of new castes in other ants, such as soldiers (modified workers) or permanently wingless gynes.

"Such novel castes often originate as mosaic phenotypes that recombine gyne- and worker traits, which may become permanent when natural selection rewards a subsequent shift in JH-sensitivity window," says Guojie Zhang, corresponding author of the study and Professor at Zhejiang University in Hangzhou and Adjunct Professor at the University of Copenhagen.

"The results confirm the strong analogy between how cell differentiation in animal bodies and caste differentiation in ant colonies works. Similar to animal breeders having not yet succeeded in using somatic cells to produce new animals, this study found similar limitations at the higher level of colonial organization in ants," concludes Professor Koos Boomsma at the University of Copenhagen, a senior co-author of the study.