Queen loss fails to elicit physiological and transcriptional responses in workers of the invasive garden ant Lasius neglectus.

Abstract

Colonies of insects with morphologically distinct castes have been called superorganisms because the function of their queens and workers is analogous to the germline and soma in metazoan bodies. In the case of formicoid ants, workers typically have lost the sperm storage organ, but they have retained ovaries. These workers can lay unfertilized eggs, which develop into males. Worker reproduction typically occurs after queen loss and involves many physiological changes, including ovary activation and an extension of lifespan. Yet, in some ant species, the workers have become sterile and the colonies have many queens that are regularly turned over. This syndrome preadapts them to become nest-budding invasive ants. We hypothesized that the combination of full worker sterility and regular queen replacement should have relaxed selection on the typical worker response to queen loss, because workers would never experience a queenless state. To test this hypothesis, we experimentally removed queens in colonies of the invasive ant Lasius neglectus. We found that queen removal indeed failed to elicit changes in fat body gene expression. Queen removal also did not increase orphan workers' stress resilience, a response observed after queen loss in ants with single-queen colonies. We did detect comparable age-related transcriptional changes in both workers and queens, which shows that our analyses were sensitive enough to detect responses to queen loss. The highly polygynous syndrome of L. neglectus colonies may thus have selected for a somatic workforce that is physiologically independent of queen presence.