Summary Ants exhibit cooperative behaviors and advanced forms of sociality that depend on pheromone-mediated communication. Odorant receptor neurons (ORNs) express specific odorant receptors (ORs) encoded by a dramatically expanded gene family in ants. In most eusocial insects, only the queen can transmit genetic information, restricting genetic studies. In contrast, workers in Harpegnathos saltator ants can be converted into gamergates (pseudoqueens) that can found entire colonies. This feature facilitated CRISPR-Cas9 generation of germline mutations in orco, the gene that encodes the obligate co-receptor of all ORs. orco mutations should significantly impact olfaction. We demonstrate striking functions of Orco in odorant perception, reproductive physiology and social behavior plasticity. Surprisingly, unlike in other insects, loss of OR functionality also dramatically impairs development of the antennal lobe where ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.

SUMMARY Social insects are emerging models to study how gene regulation affects behavior because their colonies comprise individuals with the same genomes but greatly different behavioral repertoires. To investigate the molecular mechanisms that activate distinct behaviors in different castes, we exploited a natural behavioral plasticity in Harpegnathos saltator, where adult workers can transition to a reproductive, queen-like state called gamergate. Analysis of brain transcriptomes during the transition revealed that corazonin, a neuropeptide homologous to the vertebrate gonadotropin-releasing hormone, was downregulated as workers became gamergates. Corazonin was also preferentially expressed in workers and/or foragers from other social insect species. Injection of corazonin in transitioning Harpegnathos individuals suppressed expression of vitellogenin in the brain and stimulated worker-like hunting behaviors, while inhibiting gamergate behaviors such as dueling and egg deposition. We propose that corazonin is a central regulator of caste identity and behavior in social insects.

Dominance rank in animal societies is correlated with changes in both reproductive physiology and behavior. In some social insects, dominance status is used to determine a reproductive division of labor, where a few colony members reproduce while most remain functionally sterile. Changes in reproduction and behavior in this context must be coordinated through crosstalk between the brain and the reproductive system. We investigated a role for biogenic amines in forming this connection in the ant Harpegnathos saltator. In this species, workers engage in an elaborate dominance tournament to establish a group of reproductive workers termed gamergates. We analyzed biogenic amine content in the brains of gamergates, insideworkers and foragers under stable colony conditions and found that gamergates had the highest levels of dopamine. Dopamine levels were also positively correlated with increased ovarian activity among gamergates. Next, we experimentally induced workers to compete in a reproductive tournament to determine how dopamine may be involved in the establishment of a new hierarchy. Dopamine levels rose in aggressive workers at the start of a tournament, while workers that were policed by their nestmates (a behavior that inhibits ovarian activity) showed a rapid decline in dopamine. In addition to dopamine, levels of serotonin and tyramine differed among castes, and these changes could contribute to differences in caste-specific behavioral patterns observed among non-reproductive workers. Overall, these results provide support that biogenic amines link changes in behavior and dominance with reproductive activity in H. saltator as well as drive differences in worker task performance.

A field-based climate warming experiment reveals a loss of dynamical community stability due to altered species interactions.